rebekah linder thesis v5
TRANSCRIPT
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Large Scale Screening of Publicly Available Metagenomes for Antibiotic Resistance
Introduction:
The term antibiotic began as a way to describe a laboratory effect or the action of a
chemical compound. Antibiotic can now be defined as a molecule that either kills or inhibits a
microbe. The first known detection of antibiotics was by Alexander Fleming with his discovery
of penicillin in 1928. Shortly after, in 1944, streptomycin was discovered to be the treatment for
tuberculosis. Once both of these antibiotics were being used universally, resistance strains began
to prevail [1]. Now, as the numbers of antibiotics in use increases, so does the prevalence of
antibiotic resistance.
Antibiotics, as a whole, are a huge leap in medicine. However, there are many downsides
to the overuse of antibiotics. If antibiotics are used for an extended amount of time, human gut
microbiota cannot fully recover, which leads to a change in the microbiota community [2].
According the cdc.gov, overuse of antibiotics can also lead to death or allergic reactions [3].
Finally, repeated use of antibiotics can lead to blindness [4], and perhaps worst of all, resistance.
Antibiotics use many different mechanisms and modes of actions. These can be seen in
Table 1 below (page 2).
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Table 1. Modes of action and resistance mechanisms of commonly used antibiotics [1].
Antibiotic class Example(s) Target Mode(s) of
resistance
-Lactams Penicillins
(ampicillin),
cephalosporins
(cephamycin),
penems
(meropenem),
monobactams
(aztreonam)
Peptidoglycan
biosynthesis
Hydrolysis, efflux,
altered target
Aminoglycosides Gentamicin,
streptomycin,
spectinomycin
Translation Phosphorylation,
acetylation,
nucleotidylation,
efflux, altered target
Glycopeptides Vancomycin,
teicoplanin
Peptidoglycan
biosynthesis
Reprogramming
peptidoglycan
biosynthesis
Tetracyclines Minocycline,
tigecycline
Translation Monooxygenation,
efflux, altered target
Macrolides Erythromycin,
azithromicin
Translation Hydrolysis,
glycosylation,
phosphorylation,
efflux, altered target
Lincosamides Clindamycin Translation Nucleotidylation,
efflux, altered target
Streptogramins Synercid Translation C-O lyase (type B
streptogramins),
acetylation (type A
streptogramins),
efflux, altered target
Oxazolidinones Linezolid Translation Efflux, altered target
Phenicols Chloramphenicol Translation Acetylation, efflux,
altered target
Quinolones Ciprofloxacin DNA replication Acetylation, efflux,
altered target
Pyrimidines Trimethoprim C1 metabolism Efflux, altered target
Sulfonamides Sulfamethoxazole C1 metabolism Efflux, altered target
Rifamycins Rifampin Transcription ADP-ribosylation,
efflux, altered target
Lipopeptides Daptomycin Cell membrane Altered target
Cationic peptides Colistin Cell membrane Altered target, efflux
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Antibiotic Resistance
Antibiotic resistance has spread rapidly throughout the years, and there are many factors
as to why. Antibiotic resistance genes (ARGs) occur naturally in bacteria and fungi across all
environments [5]. However, in many instances, the use of antibiotics greatly increases the
presence of these ARGs.
Agriculture is one of the most prominent sources of antibiotic resistance. Farmers often
spray antibiotics directly onto crops and/or use the manure from animals treated with antibiotics
as fertilizer for crops. This can absorb into the plant, which is then consumed by humans or
animals. The antibiotics can also absorb into the soil, which can then be washed off into rivers,
lakes, and streams, carrying ARGs to new places and affecting new populations [5]. The push for
more organic farming to replace inorganic nitrogen and phosphorus fertilizers is leading to an
increase in this transfer. Nonetheless, it has been found that ARGs are present in manure even if
the animal had not been treated with antibiotics [6]. In the food industry, antibiotics are used on
animals in order to increase size, production, and growth rates, as well as fight infection. Again,
these animals are then consumed, and the ARGs are transferred to humans [5].
Finally, humans use antibiotics in order to treat infections. The average American makes
outpatient visits twice a year, and 15.3% of those visits end in them receiving an antibiotic
prescription. About 100,000-200,000 tons of antibiotics are used annually, with 25,000 tons of
that total being used in China [7]. Even when a new antibiotic is introduced, its resistance strain
emerges within a few years [2]. All of the factors stated above lead to the spread of antibiotic
resistance genes and the rise of superbugs such as tuberculosis and methicillin-resistant
Staphylococcus aureus (MRSA).
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Antibiotic resistance genes work by inhibiting cell wall synthesis, DNA synthesis, RNA
synthesis, and protein synthesis [8]. They can also inactivate the antibiotic itself. A few more
pathways include alternating the binding site, modifying the metabolic pathway, and reducing
the intracellular antibiotic accumulation. Altering the binding site of the antibiotic reduces the
capacity at which the antibiotic binds. Modification of the metabolic pathway of the antibiotic
allows the cell to avoid the antibiotic effect. In order to reduce the intracellular antibiotic
accumulation, the permeability of the cell is decrease and/or the active efflux of the antibiotic is
increased [2].
The mechanisms of antibiotic resistance genes include genetic jugglery, intrinsic
resistance, the resistome, plasmid-mediated transmission, horizontal gene transfer, and cell-cell
fusion. Genetic jugglery includes random mutations of genes, leading to modified catalysts that
contain resistance. Intrinsic resistance includes genes in a bacterial genome that have a
possibility of developing a resistance phenotype. The resistome contains bacteria that produce
antibiotics as well as the resistance to those certain antibiotics [1]. In plasmid-mediated
transmission, the resistance genes are carried and spread via plasmids [9]. Horizontal gene
transfers involve neighboring bacteria swapping genetic information with each other. There are
three types of horizontal gene transfer: transformation, transduction, and conjugation.
Transformation occurs when bacteria obtains short fragments of naked DNA. Transduction
involves bacteriophages transferring DNA from one bacterium to another. Conjugation calls for
the transfer of DNA via sexual pilus [10]. Finally, cell-cell fusion involves the merging of two or
more cells in order to combine genomes [11].
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Metagenomics
Metagenomics allows for the characterization of microbial populations using its genetic
composition. It can also determine the function of microbes, as well as their evolutionary profile.
This is done by taking a sample, extracting, sequencing and then analyzing the DNA.
Metagenomics has quickly become the standard tool used by scientists in the microbial ecology
field, mostly due to its simplicity, along with its accuracy [12].
MG-RAST
MG-RAST stands for Metagenomic Rapid Annotation Using Subsystems Technology. It
is a SEED-based server hosted by Argonne National Laboratory that contains the metagenomic
information about various microbial populations. Users can upload raw metagenomic data for
analysis. According to mcs.anl.gov, MG-RAST provides the annotation of sequence fragments,
their phylogenetic classification, functional classification of samples, and comparison between
multiple metagenomes. MG-RAST also allows for the configuration of initial metabolic
reconstruction for the metagenome [13].
Comprehensive Antibiotic Resistance Database
The Comprehensive Antibiotic Resistance Database, or CARD, is a database that
includes data about antibiotics as well as antibiotic resistance genes and their associated proteins.
The CARD helps to classify antibiotic resistance gene data. It contains tools that help identify
antibiotic resistance genes from either partial or whole sequence data [14].
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rpoB
rpoB is a gene that encodes the beta subunit of RNA polymerase [15]. It is a single-copy
protein encoding gene that is used as a marker for pyrosequencing-based assessments of
bacterial diversity in soil. [16].
USEARCH & UBLAST
USEARCH and UBLAST are algorithms that are used to search sequence databases.
They do this by pursuing high-scoring global and local alignments. UBLAST has been proven to
be up to 350 times faster than NCBI BLAST (another widely used algorithm) with similar or
even higher sensitivity [17].
Objectives
Because of the lack of consistency in using metagenomics to study antibiotic resistance
genes, this study researched any correlation there could be with the prevalence antibiotic
resistance in certain environment types. In order to do this, information from the MG-RAST
server will be compared to the CARD database.
The goal of this project is to create a reference between ARGs and MG-RAST available
datasets that could potentially give rise to a wider understanding of the source of ARGs in the
environment. This experiment could also create a profile of certain ARGs using environmental
information, ARG abundance, phylogenetic/taxonomic abundances, and metabolic pathways,
which could lead to new understandings of the distribution of ARGs in the environment.
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Materials and Methods:
Sampling and Data Sources
Data sets (1,056) were selected randomly, and downloaded directly from MG-RAST
using the MG-RAST API. The larger dataset was trimmed to 374 metagenomes based on the
ability to identify the sample type and quality of data (Table S1). There were 11 total
environment types: air (n=5), animal (n=50), coral reef (n=13), grassland (n=3), human (n=134),
mangrove (n=9), marine (n=23), soil (n=98), tundra (n=3), wastewater (n=11), and water (n=25).
The total amount of base pairs for this dataset was 2.15E11, and the total number of sequences
was 1.38E9. The largest sample had 7.04E9 base pairs and 6.98E7 sequences and belonged to a
human environment. The smallest sample had 3.10E6 base pairs and 9433 sequences and
belonged to a human environment as well.
Resistance Gene Detection
Because MG-RAST does not contain information on ARGs, the data sets had to be
compared against the Comprehensive Antibiotic Resistance Database (CARD). The screen-
passed data (DNA sequence data of acceptable quality and predicted as gene coding regions by
MG-RAST) from MG-RAST was searched against CARD in order to detect ARGs as well as
rpoB gene copies, or gene copy fragments. UBLAST and USEARCH algorithms [17] were used
to search the CARD database with the following search parameters: the e-value used was 1E-5,
with minimum 80% similarity using local alignments. Only 374 data sets were used in this
experiment, as samples were removed if the results were 5 kb or less (as they would only contain
a few hundred hits), or if there was only one sample from a certain environment type. The
samples were normalized by dividing the copy number of each ARG category by copy numbers
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of rpoB. This was done because it gives a more accurate representation of amount of ARGs in a
sample with respect to the number of prokaryotes. In the past, other studies [18], [19] divided by
the amount of 16s rRNA genes, but rpoB has a higher genetic resolution and reports more
species [16].
Statistical Analysis
R was used to analyze the data. The base R libraries, vegan, and gplots were used to
graph relative abundance heat maps (Figures 1 and 2), relative abundance of ARG categories
containing all samples (Figure 3), amount of rpoB copies per million base pairs (Figure 4), and
amount of ARG copies per rpoB copies for specific ARGs (Figures 5-8). Clustering of
environments by ARG categories was performed using Bray-Curtis dissimilarity with the
UPGMA algorithm and either median values by environment, or all data (Figures 1 and 2,
respectively).
Results and Discussion:
In Figure 1, the median value of the efflux pump conferring antibiotic resistance gene
was the most abundant across all environments, with mangroves, air, and wastewater having the
highest abundance. Animals, marine, and water environments had the lowest abundance. This is
because efflux pumps are in both Gram-negative and Gram-positive cells, along with eukaryotes.
In Figure 2, the beta-lactam resistance gene shows the highest abundance, followed by
the antibiotic inactivation enzyme. The least abundant gene was antibiotic sequestration. Human
saliva showed the highest amount of antibiotic resistance genes, with the beta-lactam resistance
gene being the highest, followed by the antibiotic inactivation enzyme.
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Figure 3 demonstrates the mean of each antibiotic resistance gene copy per rpoB copy.
The beta lactam resistance gene had the highest mean, but the antibiotic inactivation enzyme had
the greatest range. The efflux pump conferring antibiotic resistance contained the highest median
value. The resistance gene with the lowest amount of ARG copies/rpoB copies was the gene
involved in antibiotic sequestration.
The effective genome size is 6.3 million base pairs (mbp) for soil, 4.7 mbp for bacteria,
and 1.6 mbp for water [20]. The results in Figure 4 are lower due to the exclusion of DNA that
does not belong to ARGs. Air had the highest amount of rpoB copies per million base pairs,
while mangroves had the lowest. Soil had the greatest amount of variance amongst the
environments; however, humans had the highest number of copies per million bases pairs.
Although humans had the largest range of gene copies in Figures 5-8, humans had a much
larger ratio in Figure 6 because beta lactam are the most widely used group of antibiotics, which
gives rise to resistance genes. Mangroves had an unexpected high amount of resistance gene
copies per rpoB copies. This could be due to the fact that these particular samples were taken
from mangroves that had been exposed to long term fertilization, which undoubtedly contained a
massive amount of antibiotics. The resistance gene copies per rpoB copies was expected to be
high in air, as the source of these samples were pig farms in South Korea. Water had the lowest
range of gene copies throughout Figures 5-8, except for Figure 6, where animals had the lowest
ratio.
For future projects, in order to test the accuracy of the methods, a known sequence could
be taken, mutated, and then inserted into an MG-RAST sample to see if it can be detected. More
samples from more diverse environments could also be used in order to get a larger variety.
Finally, implementing an environmental organizational standard would greatly benefit future
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researchers for projects like this one, so that results are more consistent and accurate across the
board.
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Figures and Tables:
Figure 1: Relative Abundance of ARGs by Environment Type
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Figure 2: Relative Abundance of ARGs by Sample ID
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Figure 3: Relative Abundance of ARG Categories Containing All Samples
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Figure 4: Amount of rpoB Copies per Million Base Pairs
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Figure 5: Amount of Macrolide Resistance Gene Copies per rpoB Copies
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Figure 6: Amount of Beta Lactam Resistance Gene Copies per rpoB Copies
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Figure 7: Amount of Erythromycin Resistance Efflux Pump Gene Copies per rpoB Copies
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Figure 8: Amount of Efflux Pump Conferring Antibiotic Resistance Gene Copies per rpoB
Copies
Additional File: Table S1
Table S1
mgm_IDaminocoumarin.resistance.geneaminoglycoside.resistance.geneantibiotic.inactivation.enzymeantibiotic.resistance.gene.cluster..cassette..or.operonantibiotic.resistant.gene.variant.or.mutantantibiotic.target.modifying.enzymeantibiotic.target.protection.proteinantibiotic.target.replacement.proteinbeta.lactam.resistance.genechloramphenicol.resistance.geneefflux.pump.conferring.antibiotic.resistanceelfamycin.resistance.geneerythromycin.resistance.efflux.pumpethambutol.resistance.genefluoroquinolone.resistance.genefosfomycin.resistance.genefusidic.acid.resistance.genegene.altering.cell.wall.charge.conferring.antibiotic.resistancegene.conferring.antibiotic.resistance.via.molecular.bypassgene.conferring.resistance.via.absencegene.involved.in.antibiotic.sequestrationgene.involved.in.self.resistance.to.antibioticgene.modulating.antibiotic.effluxgene.modulating.beta.lactam.resistancegene.modulating.permeability.to.antibioticglycopeptide.resistance.geneisoniazid.resistance.genelincosamide.resistance.genelinezolid.resistance.genelipopeptide.antibiotic.resistance.genemacrolide.resistance.genemupirocin.resistance.genenitrofuratoin.resistance.genepeptide.antibiotic.resistance.genephenicol.resistance.genepleuromutilin.resistance.genepolyamine.resistance.genepolymyxin.resistance.genepyrazinamide.resistance.generifampin.resistance.genestreptogramin.resistance.genestreptothricin.resistance.genesulfonamide.resistance.genetetracycline.resistance.genetriclosan.resistance.genetrimethoprim.resistance.genetunicamycin.resistance.generpoBrpo_mbpinterestdownloadedidprojectnamebpssequencesEnvironment_combinedbiomefeaturematerialenviroment.nbsp.packagedisease_statussequencing.nbsp.typelocationphcountrytemperaturesequencing.nbsp.methodavg.nbsp.seq.nbsp.lengthNA.
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mgm44411440.250.3790322580.0322580650.3870967741.17741935500.1693548390.0403225810.4516129030.2822580651.1774193550.4435483870.02419354800.725806452000.1612903230.3225806450.06451612900.4435483870.47580645200.0161290320.29838709700.024193548000.2500.1290322580.04838709700.0403225810.0241935480.16129032300.2258064520.04838709700.0645161290.5322580650.0564516130.04032258101241.5044084141426584441144.3Global Ocean Sampling ExpeditionGS010 Shotgun - Coastal - North American East Coast - Cape May, NJ - USA8242442678304Marinemarine habitatmarine habitatmarine habitatwaterNAWGSCape May, NJNAUnitedNAStatesNAofNAAmerica12other1052.621public
mgm44411480.6341463410.6829268290.3414634150.6829268292.8292682930.2439024390.2926829270.0487804881.121951220.6585365852.9024390240.6585365850.0487804880.2926829271.707317073000.3902439020.5121951220.17073170700.7317073171.24390243900.0731707320.4878048780.2195121950.12195122000.92682926800.3414634150.1219512200.0487804880.0243902440.3902439020.0731707320.5365853660.14634146300.1707317070.9512195120.2439024390.0487804880410.7488296981426584441148.3Global Ocean Sampling ExpeditionGS117b Shotgun - Coastal sample - Indian Ocean - St. Anne Island, Seychelles - Seychelles5475210250609Marinemarine habitatmarine habitatmarine habitatwaterNAWGSIndian Ocean - St. Anne Island, SeychellesNASeychelles26.5other1081.865public
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mgm44415680.06250.2291666670.0833333330.3854166670.531250.0104166670.156250.0104166670.2916666670.0729166670.6250.270833333000.3020833330.01041666700.0520833330.3750.01041666700.2708333330.14583333300.0208333330.36458333300.03125000.0937500.0208333330.02083333300.0104166670.0104166670.05208333300.0729166670.02083333300.0208333330.36458333300.0104166670961.4756546041426584441568.3Global Ocean Sampling ExpeditionGS119 Shotgun - Open Ocean - Indian Ocean - International Water Outside of Reunion Island - International6505587460987Marinemarine habitatmarine habitatmarine habitatwaterNAWGSIndian Ocean - International Water Outside of Reunion IslandNAunknown23.8other1066.717public
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mgm44415851.0808823531.0661764710.2058823530.4338235292.8602941180.0735294120.3529411760.1029411761.6176470591.3161764714.0147058820.7867647060.0955882350.0882352942.91911764700.0147058820.4632352940.1838235290.25735294100.6911764711.78676470600.0220588240.1397058820.0661764710.051470588001.2867647060.0514705880.5147058820.11029411800.0294117650.0441176470.7205882350.0220588240.6691176470.05882352900.2573529411.5073529410.1102941180.63970588201360.9127052831426584441585.3Global Ocean Sampling ExpeditionGS013 Shotgun - Coastal - North American East Coast - Off Nags Head, NC - USA149007574138033Marinemarine habitatmarine habitatmarine habitatwaterNAWGSOff Nags Head, NCNAUnitedNAStatesNAofNAAmerica9.3other1079.507public
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