virology in the classroom: current approaches and

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Virology in the Classroom: Current Approaches and Challenges to Virology in the Classroom: Current Approaches and Challenges to

Undergraduate- and Graduate-Level Virology Education Undergraduate- and Graduate-Level Virology Education

David B. Kushner Dickinson College

Andrew Pekosz

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Recommended Citation Recommended Citation Kushner, David B., and Andrew Pekosz. "Virology in the Classroom: Current Approaches and Challenges to Undergraduate- and Graduate-Level Virology Education." Annual Review of Virology 8 (2021): 537-558. https://www.annualreviews.org/doi/citedby/10.1146/annurev-virology-091919-080047

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Annual Review of Virology

Virology in the Classroom:Current Approaches andChallenges toUndergraduate- andGraduate-Level VirologyEducationDavid B. Kushner1 and Andrew Pekosz21Department of Biology, Dickinson College, Carlisle, Pennsylvania 17013, USA;email: [email protected] of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg Schoolof Public Health, Baltimore, Maryland 21205, USA

Annu. Rev. Virol. 2021. 8:537–58

First published as a Review in Advance onJuly 9, 2021

The Annual Review of Virology is online atvirology.annualreviews.org

https://doi.org/10.1146/annurev-virology-091919-080047

Copyright © 2021 by Annual Reviews. This work islicensed under a Creative Commons Attribution 4.0International License, which permits unrestricteduse, distribution, and reproduction in any medium,provided the original author and source are credited.See credit lines of images or other third-partymaterial in this article for license information

Keywords

microbiology, virology, education, undergraduate, graduate, inclusivity

Abstract

The pervasive effects of the current coronavirus disease 2019 pandemic arebut one reason for educators to refocus their efforts on virology teaching.Additionally, it is critical to understand how viruses function and to elucidatethe relationship between virus and host. An understanding of current virol-ogy education may improve pedagogical approaches for educating our stu-dents and trainees. Faculty who teach undergraduate microbiology indicatethat approximately 10% of the course content features viruses; stand-alonevirology courses are infrequently offered to undergraduates. Fortunately, vi-rology taught to undergraduates includes foundational material; several ap-proaches for delivery of lecture- and lab-based content exist. At the graduateeducation level, there is growing appreciation that an emphasis on logic, rea-soning, inference, and statistics must be reintroduced into the curriculum tocreate a generation of scientists who have a greater capacity for creativityand innovation. Educators also need to remove barriers to student success,at all levels of education.

537

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1. INTRODUCTION

Why did we become interested in learning about and studying viruses?Was it to attempt to betterunderstand disease-causing agents and pathogenic mechanisms or the relationship between virusand host cell? Can we even remember what drew us to this field? This line of questioning leadsto still more questions: What might drive an undergraduate student to want to study virology?What should those who teach undergraduates try to communicate to the students enrolled in ourclasses? What is the pipeline for getting students to graduate school in virology? What are thegoals of the trainees? How can we assist our students in meeting their goals? While there mightbe several answers to these questions, one thing is clear: there is a need to help people betterunderstand and appreciate science as a first step toward improved attitudes and engagement.Quickglances through Facebook and Twitter reveal the anti-science sentiment currently prevalent in theUnited States and in several other parts of the world. The coronavirus disease 2019 (COVID-19)pandemic has thrust virology into the spotlight and, for better or for worse, has illustrated thecomplex interplay between science and society. Therefore, virology education is as important asever. (See the sidebar titled Why Learn Virology?)

Keeping students engaged with science, and helping them recognize science’s value, as an in-tegral part of their education is one way to help improve public support of science. Introducingstudents to virology throughout their education can help generate excitement about the field.However, at the undergraduate level, most students are not exposed to much virology content,even in microbiology courses. Virology educators need to help undergraduate faculty who mayhave little background in virology find ways to incorporate more virology-based content into rel-evant biology courses. This could better introduce undergraduates interested in virology to thesubject and begin to prepare them for careers in this field. Challenges in virology education arefound not just at the undergraduate level; there are challenges at the graduate level as well. Anascent desire to reintroduce philosophy into doctor of philosophy (PhD) programs will bring agreater emphasis to identifying novel problems and approaches to address virology research. Thegrowing use of preprints also highlights the need to emphasize the critical reading and analysis ofarticles that now must occur before the traditional path of peer review has been completed.

In this review, we focus on several aspects of virology education: illuminating the access to vi-rology that exists at the undergraduate level, describing several peer-reviewed virology lecture andlab exercises that could be integrated into undergraduate coursework, considering what students

WHY LEARN VIROLOGY?

Viruses are often studied because they can cause disease. The eradications of smallpox in 1980 and rinderpest in2011, coupled with the control of major diseases such as measles and polio, have had a profound effect on humanhealth and lifespan, and the coronavirus disease 2019 pandemic has captured the entire world’s attention. We alsocannot ignore viral diseases of plants and insects. Although studying viruses and disease is important, we need tobetter understand—and appreciate—that virology is about more than disease. Virologists were the first to show thatnucleic acids (not proteins) transferred hereditary information; basic research into viruses has been fundamental toour knowledge of cell and molecular biology, biochemistry, and biotechnology, as evidenced by ∼25 Nobel Prizes.Viruses are everywhere and infect everything. They make up the largest amount of biomass in our oceans, buttheir role in ocean ecology is quite unclear.While the bacteria that compose our microbiome are being categorizedextensively, research on the viruses that compose our even more diverse virome is still in its infancy. Introducingstudents to virology early in their education will help us attract new talent to continue our efforts to understandviruses.

538 Kushner • Pekosz

might learn about virology prior to college-level study, and examining new approaches to virologyeducation at the graduate level. In addition, some challenges our students and trainees face duringtheir education are considered to help raise awareness of how faculty and mentors can serve asallies.

2. VIROLOGY IN HIGH SCHOOL

While this review focuses mainly on undergraduate and graduate education in virology, asI (D.B.K.) was thinking about what undergraduates learn, I wondered if I learned any virologyduring high school. In my high school biology textbook (1), I found Chapter 11: “Viruses andMonerans.” The properties, size, and shape of viruses were described in about 5 pages of text andfigures, and the text also noted a very little bit about phagocytes and antibodies as ways to protectagainst viral infection. Latency, the link between some viruses and cancer, and cell death werementioned as possible outcomes of viral infection. Reproduction of viruses was exemplified usinglytic bacteriophage, and there was a brief mention that animal viruses enter cells by attachmentto a cellular receptor and that replication of new animal viruses does not always cause cell death.So, these few pages in the textbook provided a brief introduction to virology.

Because that experience was 35 years ago, examination of current practices in regard to highschool virology was warranted. I reached out to the Advanced Placement (AP) Biology teacherat our local high school. Pennsylvania uses its own Keystone exams to assess student learning. Inour local school, there used to be an entire microbiology unit in Biology I. But, due to the currentKeystone standards, which mention the word “virus” only once (“compare and contrast a virus anda cell”) in a nearly 500-line spreadsheet of content to be covered, teaching of viruses is basicallynonexistent. AP Biology guidelines, which are not subject to the Keystone standards, do recom-mend the teaching of what is a virus, the virus life cycle, immune system function, and vaccines.

On the other side of the virology content spectrum, some science-specific high schools offermuch more. For example, the Illinois Math and Science Academy (IMSA) is a selective residentialpublic school for Illinois tenth through twelfth graders. Due to the science focus, there are anumber of current courses with virology content. In the class Advanced Biological Systems foreleventh graders, the evolution unit features content about the origins of viruses and cellularlife, and an examination of the hemagglutinin (HA) and neuraminidase (NA) genes of influenzausing protein sequence alignment and phylogenetic trees. In the twelfth-grade elective courseMicrobes and Disease, a unit on viral pathogenesis examines the life cycles and other features ofpox-, influenza, and dengue viruses. Students at IMSA also have the option to take a year-longresearch-based course to isolate and characterize bacteriophages, modeled after the Science Edu-cation Alliance Phage Hunters Advancing Genomics and Evolutionary Science (SEA-PHAGES)program (see Section 3.5.2). Elsewhere, in a report from a few years ago, what Austrian seventhand tenth graders (as well as university students) learned about viruses was assessed using a24-question, non-multiple-choice survey. Analysis of responses from 133 seventh graders and199 tenth graders showed an improvement in knowledge of virology concepts in the latter group,although both groups exhibited many conceptual gaps (2). Notably, these seventh and tenthgraders in Austria were being taught, and knew, some virology, and the analysis suggests anapproach we could adopt in the United States, especially in light of the ever-increasing need toeducate our students about important science topics.

3. VIROLOGY AT THE UNDERGRADUATE LEVEL

In the United States, because the amount of virology content covered in high school biologycourses typically is minimal, some questions arise: How much virology might an undergraduate

www.annualreviews.org • Virology Education 539

student learn? Are students typically exposed to virology in an introductory biology (survey)course? Are there opportunities for undergraduates to take a stand-alone virology course? Witha lab? If not, what virology is covered in a typical microbiology course?

3.1. Introductory Biology

As I (D.B.K.) perused my old high school text to revisit the virology content presented init, I similarly examined the textbook (3) we currently use for introductory biology courses atDickinson College. Although the text is appropriately updated, the amount of coverage ofviruses is not much more than appeared in my 1985 high school textbook (1). Included is a briefexplanation of viral diversity and why viruses cannot be placed on the tree of life; mini-sections onpositive-sense single-stranded RNA (ssRNA), negative-sense ssRNA, retro-, and double-strandedDNA viruses; and an introduction to phage therapy. Phages are mentioned when describing the1952 Hershey-Chase experiment (phage DNA—and not phage protein—enters bacterial cells todirect replication of new virus and therefore is the genetic material). In a chapter on regulation ofgene expression, virus replication [lytic/lysogenic cycles, human immunodeficiency virus (HIV)replication] is briefly described; in a short chapter on immunology, there is a mini-section onacquired immunodeficiency syndrome (AIDS) and immune deficiency. Therefore, in a typicalyear-long introductory biology course, students are, at best, minimally introduced to virology(although there are exceptions, as described later).

3.2. American Society for Microbiology Undergraduate Curriculum Guidelines

In 2001, an update on a 1998 document conveyed what the American Society for Microbiology(ASM) Undergraduate Education Committee recommended as curricular content for microbiol-ogy majors: an introduction to microbiology course (with lab); core courses in microbial physi-ology, microbial genetics, and microbial diversity and ecology (all with lab); an advanced coursewith lab; and a capstone course. Immunology, pathogenic microbiology, and virology were amongseveral electives suggested for microbiology majors (4). So, microbiology majors might get somevirology in their introductory microbiology course, and some of these students might get morevia recommended electives.

Updated guidelines were provided in 2012, following the 2011 ASM Conference for Under-graduate Educators Meeting, during which a subset of meeting attendees (including D.B.K.) re-viewed the guidelines. The updated guidelines use elements from the Vision and Change report(5) and encourage teaching of 27 items compartmentalized into 6 conceptual areas: evolution, cellstructure and function,metabolic pathways, information flow and genetics,microbial systems, andimpact of microorganisms (6). Thirteen skills (scientific and laboratory) also are detailed in theseguidelines. While several of the 27 items feature the broad term “microbial” (which could implybacteria, archaea, and/or viruses), only 1 of the 27 items explicitly uses the term “viruses” and2 others use the term “viral”—to recommend the learning of lytic/lysogenic replication cyclesof viruses and how those are determined by their structures and genomes, that synthesis of viralgenetic material and proteins is host-cell dependent, and that microorganisms (cellular and viral)can interact with human and nonhuman hosts in various ways that are not always detrimental.Lab competencies and skills focus on scientific thinking and hands-on skills, which can be broadlyapplied to the study of both bacteria and viruses, but typically bacteria would be studied in the un-dergraduate lab due to safety and cost. [Regarding microbiology content, it should be noted thatASM has developed separate guidelines for undergraduates in nursing and allied health programs(7); again, viruses are specifically noted only minimally.]


For most undergraduates, the likeliest scenario is that they might take one upper-level micro-biology course because they major in biology, zoology, biochemistry, or molecular/cellular biologyinstead of microbiology, or because a microbiology major does not exist at their institution. Andbecause that one course would serve as an introduction to the discipline, most of the contentfocuses on bacteria. Therefore, how much undergraduate microbiology coursework features vi-rology? How often is virology taught as a stand-alone course at the undergraduate level? Havingsurveyed colleagues at approximately 30 small liberal arts colleges (SLACs) and primarily un-dergraduate institutions (PUIs), I (D.B.K.) next (a) overview the virology content in SLAC/PUImicrobiology courses, (b) note that virology is taught at a small subset of these schools, and(c) describe some ways in which virology-specific content has made its way into the undergraduatecurriculum.

3.3. Virology Content in Small Liberal Arts College/Primarily UndergraduateInstitution Microbiology Courses

In summer 2020, I (D.B.K.) sent a short survey to faculty who teach microbiology courses at thetop 50 SLACs, as defined by the 2019 US News and World Report rankings (from institutionalwebpages, it was determined that microbiology is taught at all but three of these colleges). Facultyfrom about 30 of these institutions replied and answered questions relating to virology content intheir microbiology course.

1. Do you include any class lectures on viruses in your microbiology class? If yes, please statehow many lectures (class hours), out of how many total lectures (total class hours), youspend teaching about viruses (please list the virology topics/content you cover). If no, whyis there no virology content in your class? Is it because (a) there is an undergraduate virologycourse taught at your institution, so you leave the virology content to that course, or (b) otherreason(s)?

2. Has the COVID-19 pandemic resulted in you wanting to include more virology in yourmicrobiology class? (And/or has it resulted in faculty in your department wishing to includemore virology somewhere in your curriculum?)

3. If there is a lab component for your microbiology class, do any labs involve use of virusesand/or study of viruses? If so, please briefly describe. At your institution, if there is a labcomponent, using viruses and/or the study of viruses, in classes other than microbiology, tothe best of your knowledge please state the course(s) and briefly describe the activity(ies).

3.3.1. Microbiology class lectures: content on viruses. Based on the responses from theSLAC/PUI faculty, all but one of the microbiology courses included at least some virologycontent (Figure 1). Half of the faculty devoted 2–7% of lectures to virology content; just underhalf devoted 10–18%. One course contained about one-quarter virology content, and one facultymember devoted about one-third of theirmicrobiology course to virology.The amount of time de-voted to virology correlates with the breadth and depth of the content covered. Across this group,in regard to content, most of the faculty indicated that they include content about bacteriophageswhen introducing transduction (part of horizontal gene transfer), and half of the faculty specificallynoted that CRISPR biology was included in their microbiology course. In these microbiologycourses,many faculty noted that basic principles of the virus life cycle were taught (some reviewingattachment/entry/replication/assembly/exit, and others focusing on lytic/lysogenic replication).Genome replication and/or virus classification also is commonly taught. About one-half of thefaculty noted that viruses and disease are taught. HIV, influenza, and polio were most commonly


Figure 1

Word cloud representing common virology content in microbiology courses taught by ∼30 small liberal artscolleges’ faculty. A total of 34 key terms/phrases were identified more than once within answers to a briefquestionnaire (see Section 3.3). More-frequently mentioned content items are shown in larger font size;items mentioned by only two faculty (bioterrorism, cancer virus, capsid, ecology, emerging infectious disease,evolution, and genome) are present in the word cloud but may be difficult to see due to their small size.

discussed; interestingly, only a few faculty noted that they taught about Ebola. A few facultymentioned that they teach about cancer-causing viruses, and another few faculty mentionednonanimal virus/disease links (unfortunately, with little virology content in microbiology courses,the importance of plant viruses and virus ecology is rarely taught). A few faculty noted thatthey mention the role of viruses when teaching about the microbiome. Several faculty notedthat viruses were mentioned in the context of treatment of infectious diseases—antivirals (Whatmakes a good drug target?) and vaccines. To summarize, in most of these microbiology courses,the (minimal) virology content highlights basic, key principles and uses examples focusing onmedically relevant content.

3.3.2. Has the COVID-19 pandemic resulted in an interest in teaching more virology?Most of the faculty addressed whether the COVID-19 pandemic resulted in an interest in teach-ing more virology (see the sidebar titled Virology Outside of Microbiology or Virology Courses).Of those who had taught microbiology in the spring of 2020, several noted that they includedcontent in real time to help students understand and contextualize aspects of coronaviruses in theemerging pandemic. Others noted that instead of talking about “X virus” to exemplify somethingvirological, they used severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Severalfaculty had not been teaching microbiology in the spring of 2020; most of these faculty indicatedthat they thought they might include SARS-CoV-2/COVID-19 content in their course the nexttime they taught it. A few faculty said that the pandemic made them (and/or their department)consider that an entire course in virology would be valuable to offer (but it might be logisticallydifficult for that to occur; see Section 3.4). Importantly, a few faculty said that they would not in-clude such content because of concerns that students had been personally affected by COVID-19,and it might be uncomfortable for them to learn about it during the course of the pandemic.

3.3.3. Do any labs feature viruses? Only about a quarter of the faculty indicated that therewas a virology element within their microbiology lab course. For this subgroup, most of the lab


VIROLOGY OUTSIDE OF MICROBIOLOGY OR VIROLOGY COURSES

The coronavirus disease 2019 (COVID-19) pandemic has made virology more visible, but the importance and rel-evance of viruses can be taught in courses other than microbiology or virology. Virus ecology—for example, asrelevant to the 2002–2003 severe acute respiratory syndrome and current COVID-19 outbreaks—could be part ofecology, evolution, or introductory biology courses. First-year seminar-type courses could feature aspects of virusesand viral diseases in public health. Sociology courses could include disease and connections to discrimination/equity(for example, regarding access to health care and possibly how infectious agents can differentially impact variousdemographic groups, as has been seen with COVID-19). Infectious disease has shaped history and could be inte-grated in history courses.History of science courses, while infrequently offered at undergraduate institutions, couldfeature aspects of viral plagues and/or medical advances and their effects on society. Ethics courses could analyzehealth care and/or challenges regarding vaccination and isolation/quarantine policies. Economics courses couldconsider the impact of pandemics on business and the economy. Political science courses could contain analyses onhow pandemics intersect with the role of government. Clearly, options abound for virology content to be weavedthroughout an undergraduate curriculum; as virologists, we should help other faculty integrate such content.

work featured use of phages—either isolation of phage or titering/plating/counting. A couple offaculty noted that they had used, or currently are using, CRISPR technology in their labs, withthe recognition that this is an application of phage biology and not virology itself.

Overall, the good news is that most of these microbiology courses taught at SLACs/PUIsfeature an introduction to some key aspects and applications of virology. However, one couldargue that it is insufficient for undergraduates to have only an introduction to virology. But dueto the breadth of content to cover in any general microbiology course, it is challenging to removecontent to add in more virology. Fortunately, virology courses are taught at some colleges, asdescribed next.

3.4. Small Liberal Arts College/Primarily Undergraduate InstitutionVirology Courses

As noted in the prior section, microbiology is taught at almost all of the top 50 SLACs/PUIs.However, virology is taught at just one-third of these institutions, and a lab component is presentin only a few instances. The reasons for the lack of virology courses at these institutions include(a) not having faculty with the relevant experience to teach such a course, (b) not having enoughfaculty in order to devote teaching credits to be able to offer a stand-alone virology course, and(c) not having sufficient resources (financial and/or physical space) to offer a lab component for avirology course. Several faculty in institutions where virology is not taught as a stand-alone coursedid note that in light of the COVID-19 pandemic, trying to add virology (more content within amicrobiology course or possibly offering a semester-long virology course) to their curriculum isimportant.

As I (D.B.K.) gathered through communications with several faculty who teach virology atthese colleges, along with course descriptions posted to websites, most of these courses fea-ture the virus life cycle along with connected topics (e.g., pathogenesis, viruses and cancer, im-mune response/evasion, vaccines, emerging viruses, subviral agents, gene therapy/therapeutics) asthe focus of the course. Just a few courses are organized by virus or virus class. (Another few fea-ture both life cycle and then virus families.) A few of these courses are specific to HIV biology(and include connections between science and society, and/or link biology to public health).


A few SLAC faculty report that their virology course has a lab (as noted above, this is the excep-tion rather than the rule).One faculty member noted that their lab is a semester-long investigativeproject where students use bioinformatics to identify potential amino acids of interest in the M1gene of reovirus, use plasmid mutagenesis to introduce alanine substitutions into plasmids usedfor reverse genetics, build mutant viruses via reverse genetics, and then propagate and explore thephenotypes of the mutant viruses using replication and other immunofluorescence/reporter as-says. Another faculty member noted that students do two half-semester projects: (a) isolating andcharacterizing a bacteriophage from nature, and then running a self-designed experiment to testif the phage can reduce or stop biofilm formation; and (b) learning about epidemiology througha case study. The use of phage to expose students to hands-on virology work is common, as otherSLAC faculty have indicated that they use phage when it is possible for students to perform labwork (see Section 3.5.2 for peer-reviewed examples of phage labs, as well as some other in-labvirology activities). Although I (D.B.K.) do the following in an RNA course (and not in a virologycourse), in order to examine sequence-structure-function relationships in a satellite RNA ofTurnipcrinkle virus, upper-level students perform an in vivo application of SELEX (systematic evolutionof ligands by exponential enrichment). Throughout the semester, students complete two roundsof selection in turnip plants, and then they clone, sequence, and analyze the viral RNA and oftenare able to find just a few highly functional molecules from the initial pool that persisted afterthose two rounds. Students learn multiple molecular biology techniques, and because of the tworounds of work, learning is reinforced by repeating those methods. Several students from the classsuccessfully continued these projects in the research lab (8–10). Furthermore, working with thisplant virus system is safe for students (for more about safety, see Section 3.5.2).

Because lab is not always an option, faculty often choose to supplement their courses withbooks (such as Spillover: Animal Infections and the Next Human Pandemic and And the Band PlayedOn) and commonly with extensive use of the primary literature in the form of journal clubs,writingassignments, or individual oral presentations (for peer-reviewed examples of the use of primaryliterature, see Section 3.5.1). Several faculty reported students reading 6–8 different pieces ofprimary literature during the course of the semester, and it was common for faculty to note thatthe literature assigned ties closely with the specific topic being covered in lecture at that time.In advance of a class meeting where we discuss a paper, I (D.B.K.) ask students to write abouttwo figures from a piece of primary literature. For each figure, students identify the experimentalquestion, briefly overview the method(s) employed, quantitatively (if possible) describe the datathey see in the figure, and define a conclusion supported by those data. This helps students delvedeeply into a few experiments from a paper, providing focus (the whole paper is reviewed in classvia student-led discussion).

One final teaching approach mentioned was the use of FluView (https://www.cdc.gov/flu/weekly/fluviewinteractive.htm) to help students learn about the math involved in vaccineefficacy, R0, and herd immunity—which, of course, is very pertinent not just during the yearlyinfluenza season; these concepts relate to other viral outbreaks as well, including the currentCOVID-19 pandemic.

It is important to reiterate that it is uncommon for undergraduate students (especially thoseat SLACs/PUIs) to take an entire undergraduate course in virology; the amount of virology in amicrobiology course will vary, but typically it is a small fraction of the course.When undergradu-ates cannot access a virology course (or when the virology course lacks a lab), students interestedin pursuing virology after college should try to get as much cell/molecular/biochemistry experi-ence as possible to build a foundation in key concepts as well as lab skills that often are used in avirology lab setting.


https://www.cdc.gov/flu/weekly/fluviewinteractive.htm

Table 1 Summary of peer-reviewed lecture- and lab-based virology pedagogy

Type of activity Summary Reference(s)Classroom quick activity Modeling antigenic shift and drift 16

Modeling virus transmission 17Reading/analyzing primary literature 18, 19

Classroom extensive work Research proposal to develop an antiviral drug 14Propose biology of a virus that could kill cancer cells 15

Laboratory molecular/cell methods applied tovirology

PCR, real-time PCR, and/or BLAST 20–22, 25Microscopy 26

Laboratory virological methods Plaque assay 22–25Titering infectious virus/TCID50 22, 25Immunocytology/ELISA 22Hemagglutination 25

Laboratory virus investigation Isolation/characterization of bacteriophages 27–34

3.5. Peer-Reviewed Virology Education Materials for Lecture and Lab

As noted above, while stand-alone virology courses at SLACs/PUIs are relatively uncommonand typically only a little virology can be communicated during a standard undergraduatemicrobiology course, there are a number of peer-reviewed lecture- and lab-based activities thatillustrate some options available for educators to help their students learn about and experiencevirology (Table 1). Before I (D.B.K.) describe these, it is important to note that for pedagogicalresearch to be published, the lecture- and lab-based activities described in such manuscripts havebeen assessed to help ensure that the learning goals (what the student should learn/understand bydoing this activity) are met. For example, for course-based undergraduate research experiences(CUREs), several options exist to monitor learning and engagement (e.g., 11). Using assessmentto demonstrate learning has occurred is a parallel process to bench science—a testable hypothesisabout learning is devised, students perform the activity, and a learning outcome (test, lab report,survey, etc.) is analyzed to monitor learning success. Demonstrating learning by use of qualityassessment strategies is important not just for publishing pedagogical manuscripts but also tohelp others understand and appreciate the value of that exercise. This can be especially importantwhen one considers the time and/or cost needed to adopt the activity (or a similar one) for useat one’s own institution; the immense educational benefit to the students typically will outweighthe effort required to implement the exercise, but it may not always be practical to do so.

3.5.1. Lecture. Some computer-based exercises have been published. Because there is no needfor lab space for these activities, these exercises could be done in the lecture portion of a virology(or other relevant) course. If a lab timeslot is available, permitting more time in a single meetingmight be advantageous, although it is not absolutely required. One example is a phylogenetics ex-ercise from an introductory bioinformatics course. Fillmer et al. (12) usedMEGA7,ClustalW, andamino acid sequences from the replicase of 28 tobamoviruses to teach students sequence align-ment and phylogenetics. This was done to help students understand evolution and the role ofphylogenetic relationships therein. A second example used a 50-min lecture period in a physicalchemistry class (13). Students used Phyre2, PyMol, UniProt, and the Protein Data Bank to com-pare influenza NA variants to NAs that have a solved structure, with a focus on the so-called 150loop located near the active site.

These two examples illustrate that activities using virus-based examples do not need to beconfined to a virology course. In contrast, the next two activities use and then extend important


concepts in virology during semester-long projects. First, Injaian et al. (14) had students developa research proposal on an antiviral drug. Four lecture periods were used: an introduction to theproject (week 3), in-class discussions based on interim knowledge acquisition (weeks 6 and 10), anda poster session for reporting findings (week 14). Outside of class time, students were expected touse scientific literature and databases to work on the project. Student teams were given a virusfor which an antiviral drug does not exist but (as a hint) for which a drug does exist to targeta different member of that virus’s family. Students also were subdivided into groups to obtaininformation about virus life cycle, high-throughput drug screens, and analysis of clinical trial data.This project allowed students to extend foundational content from a virology course to a real-world scenario. A similar concept is seen when students were asked to use a learning by designingapproach to propose the biological composition of an artificial virus that could kill cancer cells(15). Small groups of students applied concepts that are normally taught in a virology course:virus-host recognition and virus binding to cellular receptors, viral genome characteristics, howviruses can kill cells, immune response to viruses, and mutation of viral nucleic acid.

Much quicker in-class exercises to help illustrate principles of virology also have been de-scribed. In one, requiring 10 min, Lego bricks are used to model antigenic shift and antigenicdrift. Each Lego brick represents a genome segment, and each stud on each brick represents anucleotide (16). In another quick activity, the role of pollen in virus transmission throughout abeehive is shown. Glo Germ lotion is spread on macaroni that students (acting as the workerbees) carry back to a hive to hand off to other bees, and this can show spread of virus when UVlight is directed at infected hands. This activity revealed learning gains not just in viral spread butalso in how bees pollinate and socialize in a colony (17).

Use of the primary literature is an important skill for undergraduate students, especially as ithelps show the careful, incremental nature of research science. However, it takes time for stu-dents to gain comfort with how to read literature and understand the research performed. TheC.R.E.A.T.E. approach, in which students consider, read, elucidate hypotheses, analyze and in-terpret data, and think of the next experiment, has become a popular approach to help studentsimprove their familiarity with research papers, although the approach uses several papers on afocused topic from one lab to help students appreciate how research develops over time (18). Aninteresting use of the literature recently was described by Sulzinski (19) in which students wereasked to carefully read an instructor-assigned piece of primary literature in advance of the finalexam; then, during part of the exam, alone or with one other student, students were asked to an-swer questions (that require familiarity with course content) about the research described in thatpiece of literature.

3.5.2. Lab. A number of peer-reviewed pedagogical publications have reported on effective useof virology-aligned lab activities; often, these take the form of a molecular or cellular lab methodthat is applied to a virological question/system, typically (but not always) in the absence of in-fectious virus. Two published papers report on application of PCR, real-time PCR, and BLASTanalysis to a virological situation. In one, using three lab periods, students use BLAST to designPCR primers and to identify amplification targets, work on optimization of PCR, and use PCRand real-time PCR to amplify a portion of the HIV-1 env gene from a provided DNA template(20). In a second, using as few as two lab sessions (or as many as four), students obtain nasal lavagesamples, isolate RNA and synthesize complementary DNA, perform PCR and quantitative PCR,and analyze products using gel electrophoresis and sequencing/BLAST. Here, the idea is to lookfor human rhinovirus (HRV) nucleic acid in the samples, and look for any diversity in the recov-ered sequence and compare it to known HRV samples (21).


Other exercises involve the plaque assay, which is a method fairly unique to virology. Fac-ulty who teach in a biotechnology program have described a five-part lab experience designed togive practical skills to students who may pursue careers in virology labs or industry (22). Studentswork with biosafety level 2 (BSL2) biohazards with supervision fromwell-trained graduate studentteaching assistants (typically not an option for faculty at PUIs/SLACs) and tissue culture/cell linemaintenance by professional lab staff. Four key methods learned in this lab are a plaque assay forLambda phage (while comparing lysis kinetics of host Escherichia coli), titering murine leukemiavirus using NIH3T3 cells, immunocytology assay and ELISA to quantitate herpes simplex virususing Vero cells, and PCR of gB using human cytomegalovirus DNA purified from human fore-skin fibroblast cell supernatant (to determine the viral strain). In another example, a two-part labexperience uses a standard plaque assay to look at phage particles from a sewage sample and toexamine host (Enterobacteriaceae) specificity and diversity. Examination of aspects of phage therapyalso occurred as an extension of this project (23). A 15-min exercise to illustrate the concept ofplaque assays was reported by Khan & Read (24). Here, lab disinfectant (TRIGENE) was used tomimic the effect of lytic phages on bacterial lawns, so that students could analyze different patternsof plaquing. This facilitated a discussion as to how there can be different populations of bacteria(e.g., Staphylococcus aureus) in various hospital settings such that phage typing can help identifydifferent bacterial strains in health care environments.

Safety, of course, is a major concern when working with undergraduates. The BSL2 examplerelied on graduate student teaching assistants to help oversee the students, especially when directlyworking with virus. Other options exist, with safety in mind. For example, Grantham et al. (25)used a mutant influenza A virus that replicates only in a cell line that provides the essential M2protein in trans. Plaque assays, real-time reverse transcription PCR, TCID50, and hemagglutina-tion can be performed using this system. This allows students to work more safely with an animalvirus and mammalian cell culture—which is an important skill to develop—but does require BSL2conditions. Another option regarding safety is advance preparation of glass slides with enclosedmimivirus particles. Although this does not require hands-on work by the students, it allows forvisualization of virus with just a light microscope, which is not possible for most viruses (26).

Continuing with the theme of safety, possibly the most well-known, and certainly the mostextensively performed, virology-based teaching lab activity is isolation and analysis of bacte-riophages. The Phage Hunters Integrating Research and Education (PHIRE) program and itsexpansion to the Howard Hughes Medical Institute–supported SEA-PHAGES program arereviewed elsewhere (e.g., 27, 28), but the importance and utility of this lab-based experience forundergraduates is worth a brief mention here. In 2006, within a PLoS Genetics paper, Hatfull et al.(29) described how phage discovery can be used as an educational tool (high school and under-graduate students contributed to the isolation of mycobacteriophages and the sequencing andannotation of their genomes). In 2012, the power of the consortium model (students participatingin PHIRE, SEA-PHAGES, and a genetics course at a university in South Africa) was demon-strated when the complete genome sequences of 138 mycobacteriophages were reported (30). A2014 report (31) indicated how the SEA-PHAGES program could be adapted to a two-semesterlab sequence for first-year students to provide the 18 to 24 students per class an opportunity toparticipate in a real-life discovery-based lab project as their very first biology lab experience. Stu-dent teams in the first semester isolate bacteriophages, and then the genome from one phage perclass group is sequenced, such that it can be annotated in the second semester (31). This approachhas been modified such that all students in a large introductory biology course perform phageisolation, to provide a real research experience designed to help with retention and persistence inscience; in this instance, the annotation portion of the project is saved for students taking an upper-level course for majors (32). In order to increase the scientific literacy of non-STEM (science,


technology, engineering, and mathematics) majors and to enhance their understanding of thescientific process, the SEA-PHAGES program has been successfully offered as a two-semesternonmajors course (33). And finally, similar to PHIRE/SEA-PHAGES, Williamson et al. (34) re-ported a series of 10 lab exercises for isolation and purification of an environmental phage; studentsattempt to clone a fragment of the genomic DNA and sequence it to attempt to identify the phage.

3.6. Physical Spaces and Active Learning

A brief discussion about design of teaching spaces (and possible links to learning) is warranted, asthis topic has garnered quite a bit of attention over the past several years. Typical classroom andteaching laboratory spaces are shown in Figure 2. This particular classroom (Figure 2a) featureswheeled chairs, so students can move around easily, if needed. The tables, for two students, canbe connected or detached, to allow for reconfiguration if desired (for example, two tables pushedtogether to make a pod where four students can sit and directly interact). This pod concept isshown in the image of the teaching lab (Figure 2b), and it enhances student interaction as allmembers of the lab group are facing each other as they work together as a team. Facilitation ofstudent interaction is one mechanism to help support active learning, which is where instead ofsolely lecturing, the facultymember observes and guides as students work (often together) throughmaterial during in-person meetings (e.g., 5). Furniture design and layout (and additional featuressuch as whiteboards and/or smart boards) can and do provide students with interactive tools tohelp them discuss and illustrate ideas with their peers (35, 36).However, as noted byHacisalihogluet al. (36), other recent studies indicate that it is the active learning itself, whether in a high- orlower-tech classroom, that matters (37, 38). Yet, faculty must remember that students with socialanxiety (39) or disabilities (40) may be averse to certain forms of active learning.Most importantly,faculty/instructors need to continually consider who the students are and what the best ways areto help them learn, and they must ensure that students have an appropriate environment (also seeSection 5) for successful learning.

3.7. Summary: Undergraduate Virology

While the availability of virology in the undergraduate curriculum is important to consider, fac-ulty who teach this also need to determine what content their students actually need.With limitedtime available in the undergraduate curriculum to introduce virology, concepts—and application

a b

Figure 2

The classroom (a) and the teaching lab (b). While it is important for the faculty member to consider whatcontent to provide in a course and how to help students understand that content, it also is critical to reflecton who is in the classroom and/or lab and why those particular students are there.


Remembering

Understanding

Applying

Analyzing

Evaluating

Creating

Low

er-o

rder

thin

king

ski

llsH

ighe

r-or

der

thin

king

ski

lls

Developing

foundationalunderstanding

Extendingfoundational

understanding Figure 3

A representation of Bloom’s taxonomy. The goal for our students, whether at the undergraduate or graduatelevel, is to develop foundational understanding (content knowledge). We then guide students to be able toextend that understanding. For example, students should be able to work with the primary literature toconsider the significance of data; students (graduate as well as undergraduate) should also be able to generatethose data in the laboratory.

of those concepts—are more important than conveying an avalanche of facts. Bloom’s taxonomy(41) is useful here. For those unfamiliar with Bloom’s, the idea is that there are six aspects to learn-ing: remembering, understanding, applying, analyzing, evaluating, and creating. The first of thesix forms the base of a triangle or pyramid; the last forms the top (Figure 3). Students performthe first three aspects as a foundation for the deeper learning that occurs when students use thatfoundation to analyze, evaluate, and create. While a detailed discussion of the use of Bloom’s tax-onomy is beyond the scope of this review, it should be kept in mind as one considers the balancebetween content and application thereof—what kinds of core content must students learn aboutviruses in order to be able to apply that knowledge in relevant future contexts? Therefore, theexamples above that feature active learning (application of knowledge by doing), rather than justmemorizing facts, are valuable. This is because giving undergraduates a foundation to indepen-dently learn how to learn new things is necessary, considering that their access to virology contenttypically is quite limited.

4. GRADUATE TRAINING IN VIROLOGY

The COVID-19 pandemic has led to a substantial increase in coronavirus biology, and severaldepartments and graduate programs have initiated courses related to COVID-19 that involve theteaching of some basic aspects of virology.The questions that I (A.P.) received during these coursesindicated a tremendous interest but also highlighted a distinct lack of virology training in manygraduate disciplines, most likely due to the high degree of specialization that occurs quite soonafter students initiate their graduate studies. There has been a significant interest in reworkinggraduate education in the United States to reemphasize the Ph in the PhD degree. This has alsorippled into the design and structure of master of science (MS or ScM) education programs. Thedriving force behind this change stems from the belief that graduate training has become too spe-cialized, driven by dogma, lacking in rigor, and bereft of innovation/creativity due to an emphasison methods, techniques, and didactic learning of facts motivated by the very specialized researchexpertise of the thesis advisor. Johns Hopkins University has made significant efforts to reformgraduate education that have coalesced under the rigor, reproducibility, and responsibility (R3)graduate and postbaccalaureate training programs (42).


4.1. R3: Defining New Principles for Graduate Education

At its core, the R3 program seeks to empower the next generation of scientists with the skillsnecessary to perform innovative, cross-disciplinary, and impactful research by moving away froman emphasis on specializing quickly and early in one’s education and instead providing a broadeducation platform emphasizing basic tools and principles that can be applied to any scientificdiscipline. The following are three of the important driving principles for the R3 program:

� Rigor: Establishing the principles that help define reproducibility, such as an emphasis onnonredundant experimental design, and clearly identifying areas of uncertainty and limita-tions of a study are additional principles that should be embraced by investigators and notminimized or glossed over for the sake of maintaining a perception of high scientific impact(43).

� Statistics and quantitative analyses: A strong training in statistical methods and study de-sign that recognizes the inherent limitations of virtually all experimental methods wouldlessen the “search for a p< 0.05” and instead allow for the design of appropriately poweredexperiments that address important but sometimes difficult scientific questions (44).

� Logic and reasoning: In many ways, current graduate education in the life sciences is drivenby dogma and conventional methodology that define a scientific discipline but also can limitthe types of experiments that are considered acceptable or fundamental to that discipline.Through the introduction of basic tenets of philosophy, logic, and reasoning, graduate stu-dents would be provided with the tools needed to truly analyze and understand the strengthsin their discipline but also identify areas where new approaches would best facilitate thegeneration of new knowledge (45).

The R3 program is using a two-pronged approach for instituting these changes. The first is toprovide specific courses designed to teach the R3 principles in the first year of graduate education.The second is to take discipline-specific coursework and attempt to present it through the lens ofR3, as opposed to traditional didactic learning. For this discussion, the latter approach is discussedas it pertains to virology training.

4.2. Increasing the Knowledge Base of Virology for All Graduate Students

All microbiology graduate students regardless of specific terminal degree or subdiscipline shouldhave a solid working knowledge of virology. At Johns Hopkins University, my (A.P.) efforts to-ward this goal involve offering a course, Pandemics of the 20th Century, that focuses on recentpandemics (1918 influenza, HIV, hepatitis B/C virus, COVID-19) and near-pandemics (avian in-fluenza, SARS) involving viruses. The class is discussion based and student led, but it does not fol-low a traditional journal club format. The class is provided with a number of articles and readingmaterials, and the discussion leads are tasked with distilling out the critical concepts and providingthe scientific basis that justifies those conclusions. The class brings together students from differ-ent graduate programs (master of public health, MS or ScM, PhD) as well as across institutionaldepartments (Microbiology, Epidemiology, etc.) and frames each pandemic discussion around alarger, broader question. For example, in the HIV class discussion, the central theme is “Why areantiviral drugs so effective at controlling HIV disease?” and the students must draw evidence fromdifferent disciplines to effectively address the question. In this way, we convey to a wide range ofstudents the need for a basic understanding of virology but do so in a way that emphasizes theimportance of that knowledge from a public health, clinical, and epidemiological perspective asopposed to a traditional virus-centric one.


4.3. Educating the Next Generation of Virology Investigators

R3 principles can also be applied to more traditional, didactic courses, and at Johns Hopkins Uni-versity, our Advanced Virology course is an example of this. As the title suggests, this course isdesigned to provide a more in-depth understanding of virology, which had previously involvedintense didactic lectures on specific viruses with an emphasis on understanding molecular mech-anisms and virus mutations that altered replication and pathogenesis. The course was updated toincorporate R3 principles by first diversifying the faculty that provided lectures on specific top-ics. Immunologists, vaccinologists, and gene therapy investigators were brought in to introducevirus families from the perspective of how nonvirologists view those viruses. Each lecture wasthen paired with a student-led discussion session where the student was tasked with identifying anarea of research that was understudied but important for understanding the disease potential ofthat specific virus. The discussion leader then presented the justification for their choice of topic,drawing from data with that specific virus as well as from other virus families, and then discussedthe state of the literature on that topic. Again, this draws the discussion leader away from a tradi-tional journal club format and asks them to think about the important scientific questions in thefield from the perspective of finding the important questions and then moving to methods andexperiments that could address that question.

4.4. Summary: Graduate Virology

Applying R3 principles to graduate education in virology has the potential to fundamentally trans-form the training of students (42). A renewed emphasis on training MS or ScM and PhD studentsto be critical thinkers and rigorous experimentalists first and then apply those skill sets to trans-form and strengthen the nature of virology research will have far-reaching effects on the field.As more graduate programs move to an R3-based training philosophy, it will be critical to con-vey this to undergraduates so they are aware of the specific programs that have adopted theseprinciples and the fundamental differences in training that those programs can provide them.

5. RECOGNIZING ISSUES REGARDING DIVERSITYAND INCLUSIVITY IN SCIENCE

Not just for virology, but for all disciplines, education that engages and supports diverse studentsis important. At the undergraduate level at SLACs/PUIs, the percentage of women majoring inthe biological sciences has grown from ∼50% 20 years ago to∼75% today.However, this increasein the number of women in biology does not mean that gender bias has disappeared or even hasnotably improved. Also, science educators are seeing more students of color in the classroom, ascolleges strive to increase this population of students. This is important not just at the undergrad-uate level; it is important at the graduate level (and after) as well. For this reason, it is essential forthose of us involved in educating students/trainees to acknowledge that we need to do better tohelp them be in the best position to succeed. A brief overview of some key points is provided hereas a way to begin, or possibly continue, this critical conversation.

5.1. Educating and Training Women

There is an extensive literature regarding the topic of gender bias and its impacts on women inscience. While there has been improvement in this area, it is important to recognize that thisissue persists for students throughout their education and training, and continues to persist oncewomen join the faculty ranks. Roper (46) recently wrote a concise review that is a good sourcefor those who seek an introduction to this topic. In regard to education specifically, gender biasand gender stereotypes exist in students at least as young as those in secondary school, which can


affect decisions about pursuing STEM work at the undergraduate level (47). And then once atthe undergraduate level, perception of gender bias against women is the most significant factoraffecting choice of collegemajor (48). Similarly, gender bias leads to anticipation of being subjectedto discrimination, coupled with reduced sense of belonging, reducing STEM engagement amongwomen, even in STEM fields where women are the majority (49, 50).

While educators need to be careful about gender bias, students may exhibit such bias as well.Grunspan et al. (51) sought to explain why women leave undergraduate STEMprograms at higherrates than men and used a social network analysis to conclude that one reason is that men (butnot women) underestimate the knowledge and performance of the women in the class. Even whenwomen were documented to have performed better in the life- and physical-science classes at oneacademic institution, women still faced gender bias as they were not thought to be as academicallystrong as the men in these classes (52).

It is worth noting that a study was performed in which achievement gaps between women andmen in undergraduate introductory biology, biochemistry, and physics courses were not observed,and in the same study, students did not report concerns about stereotype threat. The authorssuggested that perceived differences in performance and concerns about stereotypemay be contextdependent (53).

Bias can continue after college. For undergraduates seeking to move into research technician/lab manager positions, a study revealed that both female and male principal investigator (PIs)concluded that a male applicant was more qualified than a female applicant and was offered a 15%higher starting salary, even though the study authors gave the same application (just the namediffered) to the biology, chemistry, and physics PIs (n = 127) to review (54).

5.2. Educating and Training Students of Color

Another current concern is retention and persistence of students of color. A disproportional sub-set of these students is underprepared when arriving to college, and greater efforts are requiredto support these students. Many summer undergraduate research experiences at Research I uni-versities are designed to actively recruit students of color (and students from other disadvantagedbackgrounds), which certainly helps some of them move forward to PhD programs, includingthose in virology, but undergraduate educators must continue to innovate in order to help thesestudents successfully progress through introductory and second-year curricula so that they remaininterested in the discipline and seek out the research experiences that can help them move on tograduate study. This is one of the most notable current challenges for undergraduate and grad-uate educators. Ultimately, educators need to remember that their work is to help their studentslearn and develop as people with an interest in science; the specific content that is learned is lessimportant than providing the opportunities for students to succeed.

However, the description above is a bit simplistic. The challenges here are significant. The2020 Black Lives Matter movement illustrates that we have much to fix, as noted in recent letters/editorials in Science and Cell regarding systemic racism in academia (55, 56). Along these lines, oneof the goals of Black in Microbiology [https://blackinmicrobiology.org/ (57)] is to help spurmuch-needed discussion of issues surrounding race in microbiology. As is the case with womenin science, Black students—including those as young as middle schoolers—question whether acareer in science is possible for them, even when they have a strong interest in the discipline (58).According to data from the Beginning Postsecondary Study, undergraduate students of color weremuch more likely than their White counterparts to switch from a STEM major to a non-STEMmajor (59).While there are efforts by granting agencies to help underrepresented students succeedin STEM disciplines [e.g., the National Science Foundation’s Science, Technology, Engineering,


https://blackinmicrobiology.org/

and Mathematics Talent Expansion Program (STEP) that now is the Improving UndergraduateSTEM Education (IUSE) program], these have not been adequate solutions.

Even when Black women persist with, and succeed in, science, some have reported extensivechallenges with sexism and racism (60). Faculty are essential in establishing inclusive STEM class-rooms and laboratories. As alluded to above, it is not sufficient simply to increase the numbers ofwomen and/or students of color in these spaces, and implicit bias often is one of the biggest chal-lenges to overcome. Science faculty can take cues from social science for developing approachesto enhance inclusive environments for our students (61).

5.3. Diversity and Inclusivity in Virology

After reading the above, onemight wonder what kind of (if any) specific progress has beenmade re-garding diversity and inclusivity in virology. Over the past few years, there have been some effortsto improve awareness of the lack of equity and/or illuminate areas in which progress is occurring.One example is an analysis of gender of invited speakers at four regularly held international vi-rology conferences. Kalejta & Palmenberg (62) concluded that slow improvement toward genderparity is occurring for invited speakers at these conferences; they also noted that when womenserve on speaker selection committees, there is a stronger likelihood for gender parity among theinvited speakers. Although this example focused mainly on PIs, it illustrates the important need toconsider equity at all levels through academia—and if doing so for speakers at conferences, suchconsideration needs to be occurring not just for PIs but also for postdocs, graduate students, under-graduates, and even students at the secondary and primary school level, in all aspects of their work/training.

Another example is theGordonResearchConference (GRC) PowerHourTM.During this rela-tively new feature of GRCs (including the Viruses andCells GRC), time is set aside for a discussionamong graduate students, postdocs, and PIs about challenges regarding diversity and inclusivity.Having attended The GRC Power Hour at the 2019 Viruses and Cells GRC, we (D.B.K. andA.P.) note that being able to have an open conversation about these challenges is a helpful re-minder of the importance of supporting all members of the virology community. Because GRCsare small conferences (∼200 attendees), ideally The GRC Power Hour participants will returnto their home institutions to disseminate information from those discussions, where challengesregarding diversity and inclusivity can continue to be mitigated.

At the undergraduate level, students interested in biology typically do not specialize in a sub-field (such as virology) until late in their college careers (if at all). However, the theme of sup-port for these students, as described in Section 5, remains critical and is essential. As noted inSection 5.2, several Research I universities that host summer research experiences for undergrad-uates encourage students from underrepresented groups to apply and attend. But those studentstypically need to persist in science (through their sophomore or even junior year) to obtain suchan opportunity. Furthermore, the number of those positions falls far short of student demand(and often only the most high-achieving students are invited to participate in those programs). AtSLACs, because of their small size, it is easier to give many (if not most or all) students a researchexperience (for example, at Dickinson, all biochemistry and molecular biology majors are requiredto complete at least one semester or one summer of bench research). But again, those students typ-ically are juniors and seniors because they usually acquire a baseline of biological theory prior tojoining a research lab (and because of limitations on how many students a faculty member cansupervise, along with budgetary constraints). In Section 3.5.2, the SEA-PHAGES program wasdescribed. Engaging students in actual research as part of course-based lab work as early as thefirst year of college has been shown to help make research more inclusive and help with retention


of students—including those from underrepresented groups—in science (31, 63). And participa-tion in SEA-PHAGES happens to introduce students to virology, which might help recruit morepeople into the field. But most critically, establishing a supportive learning environment coupledwith providing accessible, authentic (lab-based) experiences can help undergraduate students (in-cluding women and students of color) persist such that it will be possible for them to move on toadvanced study in virology (or other STEM disciplines of their choosing).

5.4. Summary: Diversity and Inclusivity in Science and Virology

It is clear that there still is much to be done to improve inclusivity in virology and in scienceas a whole. Indeed, the title of a recent piece in Scientific American, “Sexism and Racism Persistin Science,” offers a straightforward appraisal of our current challenges (64). While it would beimpossible to thoroughly examine the challenges regarding inclusivity in this review, we hope thateveryone will take time to read some of the current literature on this topic and work with othersto make our classrooms and our labs places where all students and trainees can excel in order tomake virology as strong a field as possible.

6. CONCLUSIONS

Undergraduate educators—whether for microbiology or for stand-alone virology courses—havedeveloped valuable opportunities for undergraduates to learn virology. However, these opportu-nities are limited, as illustrated by the minimal amount of virology content that can be includedin a microbiology course and the fact that stand-alone virology courses are not always availableto students. At the graduate education level, the rapid specialization of students into discipline-focused programs has also limited the opportunity to provide an in-depth introduction to virology.Because it can be argued that virology education is more important than ever, it is time for a groupof educators of virology to define what virology content undergraduates should learn in microbi-ology (and other relevant biology) courses and what they should learn if they can take virology.By coordinating these efforts with those aimed at redefining virology education at the graduatelevel, the dual goals of increasing general awareness of virology and training the next generationof virology educators and investigators can be streamlined. From the perspective of the academicinstitution, we hope the information in this review can serve as a starting place for this effort. Thiseffort might be enhanced by coordination with scientific societies such as the American Societyfor Virology and perhaps by integration of these preferences within the microbiology educationguidelines provided by groups such as the ASM. Defining important content and/or lab skillswould be especially useful to help undergraduate educators guide students toward graduate ormedical schools. Finally, and possibly most importantly, we all must continue to work to eliminatebias and to fully support our students to help them achieve their career goals.

SUMMARY POINTS

1. Most undergraduate microbiology courses do include virology content but typically onlyenough to serve as an introduction to virology.

2. Stand-alone virology courses are not available tomany undergraduate students (and suchcourses rarely feature lab components), but these courses do provide strong foundations;several published studies illustrate lecture- and lab-based approaches for helping under-graduates learn.


3. Reforming graduate education to emphasize more broadly applicable skill sets in R3

principles can result in a greater engagement in virology because it is a field that drawsfrom multiple scientific disciplines.

4. Faculty must recognize the need to more actively assist and support their students andtrainees—especially students fromunderrepresented backgrounds—to enhance diversityand inclusivity in our field.

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

D.B.K. thanks faculty at the following institutions for sharing information about their courses:Amherst College, Bates College, Bowdoin College, Bryn Mawr College, Bucknell University,ClaremontMcKenna College (Keck ScienceDepartment),Colgate University,Colorado College,Connecticut College, Davidson College, Denison University, DePauw University, Furman Uni-versity, Grinnell College, Haverford College, Lafayette College,Macalester College,MiddleburyCollege, Mount Holyoke College, Oberlin College, Occidental College, Swarthmore College,Union College, The University of the South, Washington & Lee University, Wellesley College,Wesleyan University, Whitman College, and Williams College; J. Wilkinson and C. Randall, re-spectively, provided information about Carlisle High School and the IMSA. A.P. thanks GundulaBosch for continuing discussions regarding R3 and virology education. The authors also thank thereviewers for their constructive suggestions regarding the manuscript.

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Palo Alto, CA: Stanford Univ. Press


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