Horizontal Gene Flow inMicrobial CommunitiesThe dynamic microbial gene pool compensates for microbial speciesclonality, presenting us with both threats and promises

Tamar Barkay and Barth F. Smets

Genetic exchanges among pro-karyotes, formerly considered onlya marginal phenomenon, increas-ingly are being viewed as pro-foundly affecting evolution. In-

deed, some researchers argue for utterlyrevamping our concept of microbial speciationand phylogeny by replacing the traditional“tree” with a newer “net” to account for thesehorizontal transfers of genes (see p. 401). Thisconceptual ferment is occurring while molecularbiologists reveal how horizontal gene transfersoccur even as microbes protect the integrity oftheir genomes. Other studies reveal the numberand diversity and abundance of genetic elementsthat mediate horizontal gene transfers (HGTs)or facilitate genome rearrangements, deletions,and insertions.

Taken together, this information suggests thatmicrobial communities collectively possess adynamic gene pool, where novel genetic com-binations act as a driving force in genomicinnovation, compensating individual micro-bial species for their inability to reproducesexually. These microbial genomic dynamicscan present both environmental threats andpromise to humans.

One major threat, for example, comesfrom the spread of antibiotic resistance andvirulence genes among pathogenic mi-crobes. Another less-documented issue in-volves transgenic plants and animals, whoseuses are being restricted because of concernsthat genes may be transferred to untargetedorganisms where they might cause harm. Apossible benefit from HGT comes from itspotential to enhance the functional diversity

of microbial communities and to improve theirperformance in changing or extreme environ-ments. Such changes might be exploited, forexample, as part of efforts to manage environ-mental pollution and might be achieved byspreading genes into resident microbes to conferspecific biochemical activities.

Discrete Steps Needed for

Stability of Gene Transfer

Stably incorporating horizontally transferredgenes into a recipient genome involves five dis-tinct steps (Fig. 1). First, a particular segment ofDNA or RNA is prepared for transfer from thedonor strain through one of several processes,including excision and circularization of conju-gative transposons, initiation of conjugal plas-mid transfer by synthesis of a mating pair-for-mation protein complex, or packaging of

• Microbial communities possess a dynamic genepool, and novel genetic combinations act as adriving force to shape genomes.

• The newly realized extent and importance ofhorizontal gene transfers will need to be integratedwith 20th-century explanations of Darwinian evo-lution.

• Horizontal gene transfers can affect human andenvironmental health and productivity— for ex-ample, by enabling pathogens to develop resis-tance to antibiotic treatments.

• Little is known about accessory and ORFangenes, even though they likely are involvedwhen microbial communities adapt to changingenvironments.

Tamar Barkay is anAssociate Professorof Microbiology inthe Department ofBiochemistry andMicrobiology, Rut-gers University,New Brunswick,N.J., and Barth F.Smets is a Profes-sor of Environmen-tal Microbiology atthe Institute of En-vironment & Re-sources, TechnicalUniversity of Den-mark, Lyngby, Den-mark. This article isinspired by a work-shop on “HorizontalGene Flow in Mi-crobial Communi-ties” that was co-chaired by theauthors in Warren-ton, Va., in June2004.

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nucleic acids into phage virions. Next,the segment is transferred either by con-jugation, which requires contact be-tween the donor and recipient cells, orby transformation and transductionwithout direct contact.

During the third step, genetic mate-rial enters the recipient cell, where cellexclusion may abort the transfer. Oth-erwise, during the fourth step, the in-coming gene is integrated into the recip-ient genome by legitimate or site-specific recombination or by plasmidcircularization and complementary-strand synthesis. Barriers to transferduring this step come from restrictionmodification systems, failure to inte-grate and replicate within the new hostgenome, and incompatibility with resi-dent plasmids. In the final step, trans-ferred genes are replicated as part of therecipient genome and transmitted todaughter cells in stable fashion oversuccessive generations.

Researchers from different disci-plines tend to focus on specific stageswithin this five-step sequence. Thus,evolutionary biologists who examinemicrobial genomes for evidence of pasttransfers tend to look at HGTs from theperspective of step five. Molecular biol-ogists are more likely to examine thedetails of the transfer events, while mi-crobial ecologists look more broadlywhen they describe the magnitude anddiversity of the mobile gene pool, some-times called the mobilome.

We believe that these perspectivesneed to be integrated if we are to de-velop an understanding of how HGT affectsmicrobial speciation, diversity, and competenceacross the multitudes of ecological niches foundon Earth. Indeed, embracing HGT may force usto revisit and revamp 20th-century efforts toexplain Darwinian evolution in the context ofMendelian genetics, particularly its central tenetregarding the vertical inheritance of genes.

What Genomes Say about HGT and Its

Impact on Microbial Communities

Comparing microbial genomes for evidence ofHGT is a retrospective approach, detecting such

events based on marks they made on DNA se-quences and on gene distributions, deletions,and insertions. Also, the presence of conflictingphylogenies between specific genes and a con-sensus phylogeny representing the majority ofthe genes in the genomes, when supported byrobust statistical analyses, suggests inheritanceof the former by HGT. The presence of atypicalgenes—those deviating in their codon usage pat-terns or G�C content—may indicate transfersso recent that the protein synthesis machinery ofthe new host has not yet affected these biases.

While such studies are consistent with ram-pant HGT, their implications for microbial spe-

F I G U R E 1

Horizontal gene transfer and its impact on the evolution of life is represented by a webconnecting bifurcating branches that complicate, yet do not erase, the tree of life. Theinset illustrates the continuum of events that lead to the stable inheritance of atransferred gene in a new host.

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ciation are hotly contested. Not all genes aretreated equally by HGT. For annotated openreading frames (ORFs), there seems to be a

relationship between predicted phenotypes anddegree of inheritance by HGT. Accessory genes,those often found in the mobilome, are trans-

For Barkay, Science Combines Dreams, Craftsmanship, and Love of Nature

Asked about what she finds appeal-ing about science, Tamar Barkaymentions its “element of dream,”her term for the creative process ofdeveloping and testing ideas to re-veal the unrecognized or unknown.“Science is full of discoveries,driven by such ‘dreams,’ and I be-lieve that, without the dream part,we would not know as much as wedo,” she says. “The importantpoint is to keep on dreaming, evenif 9 times out of 10 you eithercannot experimentally test youridea—or you find out it is wrong.As long as we can master the meansto examine our ideas experimen-tally, the only limit to where sciencecan take us is our imagination.”

Today Barkay’s scientific rever-ies take shape in the Departmentof Biochemistry and Microbiol-ogy in Rutgers University’s CookCollege, where her research fo-cuses on interactions of microbeswith mercury and on horizontalgene transfers among microbesand their role in natural microbialcommunities. Her work oftendeals with microbial transforma-tions that affect mercury.

Barkay was born on a kibbutzin the northern part of Israel, whereher parents still live. At age 14, shebegan working with dairy cattle, anexperience that, when she com-pleted her military service severalyears later, prompted her to enteragricultural school. “All kids on thekibbutz at that time were to spend acouple of hours a day helping outon the farm, or in providing ser-vices to the community,” she ex-plains. “I simply chose the cows

instead of working in the kitchen,or other such duties.”

During her sophomore year incollege, she became “totally en-chanted” with biochemistry andgenetics, particularly when thetwo were merged to describe geneexpression and protein synthesis.“I was struck by the beauty of itall, by the logic and efficiency ofhow such complex processeswork,” she says. “I could see howthe two fields complement andfeed each other—remember thatthis was in the ’70s, when molec-ular biology was in its infancy.”

When an opening became avail-able in the department of plantpathology, she joined as an un-dergraduate assistant. “From thebeginning I liked the combinationof intellectual activity with crafts-manship, and with the love of na-ture which, to me, are at the core ofwhat I love about my profession,”she says.

Barkay is one of three daugh-ters of a historian—her father—and a teacher—her mother, who,since retiring, has owned a smallbookbinding shop. There are noother research scientists in thefamily; one sister develops com-puterized education systems, andthe other is a psychotherapist.

Barkay says that her attraction toscience came relatively late. “I wishI could say that I knew that Iwanted to be scientist since kinder-garten, but really this was not thecase with me,” she says. “In fact, upuntil I finished high school, I wastotaly focused on the social sci-ences, and I still remember how

much I dreaded lab classes, duringwhich I would wander around thelab being totally bored.”

Nevertheless, she became inter-ested in the academic life datingfrom a 9th-grade class visit to He-brew University in Jerusalem.“When the tour guide asked whoamong us kids was planning to goto university, I was the only onewho raised her hand,” she recalls.“One has to realize that, at thattime, you were not expected tobecome a scholar if you were bornon a kibbutz and, indeed, only afew among the 40 students in myhigh school class ever pursuedhigher education.”

She received her B.Sc. degreefrom the school of agronomy atthe Hebrew University in Rehovotin 1974, followed by her M.Sc. inenvironmental health from theHebrew University in Jerusalemtwo years later. She left for theUnited States soon after, and hasbeen here ever since.

“When I was about to finish mymaster’s degree, I wrote to about12 people asking if I could workwith them for a limited period oftime,” she says. “Rita Colwell,one of only two who responded,wrote: ‘I have money for you forsix months, if you want to come,come.’ Those initial six monthsstretched—first to five years, dur-ing which I finished my Ph.D. atthe University of Maryland—andnow to almost 30 years.”

Marlene Cimons

Marlene Cimons is a freelance writerin Bethesda, Md.

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ferred often. These genes are subject to strongselective pressure, undergo frequent transfers,and often do not produce phylogenies that canbe related to those of their host genomes.

Among genes that are less frequently trans-ferred than those in the mobilome are thoseencoding major metabolic functions, such as thesynthesis of amino and fatty acids. These “oper-ational” genes, in turn, have more frequentlyevolved by HGT than have “informational”genes, those encoding DNA replication, tran-scription, and translation. This distinction be-tween HGT of operational and informationalgenes was developed by Jim Lake and his collab-orators at the University of California, Los An-geles, who analyzed 312 groups of orthologousgenes in four bacterial and two archaeal ge-nomes. Informational functions are mediated bycomplex structures, such as ribosomes, requir-ing interactions among large numbers of pro-teins, while operational functions involve pro-teins that partake in fewer interactions. Hence,the impact of HGT on the evolution of a partic-ular gene is related to the complexity of theinteractions of its product.

Gene transfers are more likely when they oc-cur between closely related organisms with sim-ilarities in genome structure and the mecha-nisms that control recombination, replication,and gene expression, according to Jeffrey Law-rence and his collaborators at the University ofPittsburgh in Pittsburgh, Pa. However, this bar-rier may be weakened in mutator strains having adefective DNA mismatch repair, according to Jef-frey Townsend, now at the University of Connect-icut in Storrs.

Lake and his group used parsimonious treereconstructions for 20,000 genes drawn fromthe genomes of four bacteria and four archaea toshow that organisms that share ecologicalniches are more likely to exchange genes thanthose that do not. The discovery of archeal genesin the genome of the thermophilic bacteriumThermotoga maritima, and conversely, the ex-tensive presence of bacterial genes in the genomeof the mesophilic methanogen Methanosarcinamazei, support the importance of a shared eco-logical niche as a boundary to HGT.

Other evidence for the extensive role of HGT inshaping microbial communities comes from envi-ronmental metagenome sequencing projects. Forexample, Forest Rohwer and colleagues from Cal-

ifornia State University in San Diego find manymobile elements of archaeal and bacterial genes inenvironmental viral genomes (step 2 in Fig. 1). Theinvolvement of phage-mediated HGT and recom-bination is also suggested by phage signatures andfrequent recombination sites in the metagenomeof an acidophilic community currently assembledby Jillian Banfield of the University of California,Berkeley. Likewise, the genomes of the SargassoSea community include several large plasmids, ac-cording to Craig Venter of the J. Craig VenterInstitute in Rockville, Md., and his collaborators.

How Are Genes Transferred

within Communities?

One approach for measuring HGT within mi-crobial communities is retrospective and doesnot directly address the dynamics of the HGT

GlossaryAccessory genes: Genes that specify func-tions that are required under unique condi-tions rather than for the general metabolismof the organism. Often such genes encodefor resistance to antimicrobial agents, utili-zation of exotic growth substrates, orpathogenic traits.

Operational genes: Genes encoding cen-tral metabolic functions such as the synthe-sis of macromolecules, cell wall compo-nents, secondary metabolites, and energyproduction.

Informational genes: Genes specifying in-formation storage and processing, such asDNA replication, transcription, and trans-lation.

ORFan gene: An open reading framewhose putative product has no homolog indatabases and whose function is unknown.

Transferant: An organism whose genomehas been modified by the acquisition of for-eign DNA or RNA regardless of the mecha-nism by which this gene transfer occurred. Itis inclusive of several terms, includingtransconjugant, transformant, and trans-ductant.

Mobilome: That part of the genome that isintrinsically mobile (e.g., plasmids), can easilybe made mobile (e.g., integrated conjugativeelements, genomic islands), or is the result ofidentifiable horizontal transfer event (e.g.,genomic island).

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process. A second approach detects ongoingHGT in intact or manipulated microbial com-munities, including conjugal plasmid transfer

from donor bacteria to recipients in microcosms(Fig. 2). For instance, Acinetobacter spp. serveas model recipient organisms for both intra- andinterspecies gene transfers by transformation in-volving biofilms and simulated soil communi-ties. Other studies suggest that competency—the phase during which cells can take upexogenous DNA—is much more common thanwas once surmised, highlighting transformationas a mechanism of HGT in the environment.Meanwhile, transduction is another processleading to genetic innovation in aquatic andterrestrial environments where viral abundanceexceeds that of the prokaryotic biomass by 10 to1.

Other efforts focus on compiling inventoriesof the environmental mobilome. For example,John Fry from Cardiff University “captures”conjugal and mobilized plasmids from microbesin undisturbed communities by “seeding” theirenvironment with marked recipient strains.Others use this approach to collect novel plas-mids from various environments. Similar toolsare used to capture transposons and integrons.The emerging picture shows an immense, possi-bly ecosystem-specific, diversity. For example,Patricia Sobecky and collaborators at the Geor-gia Institute of Technology in Atlanta describenovel origins of replication in plasmids frommarine bacteria. Likewise, Hatch Stokes and hiscollaborators from Macquarie University inSydney, Australia, studying integrons in soilDNA extracts, suggest that these elements arekey players in the evolution of microbial com-munities. How these elements may modulatemicrobial evolution is exemplified by theTn4371 element in Ralstonia sp. A5, which wasrecently reclassified as a genomic island by Ad-riane Toussaint and coworkers at the UniversiteLibre de Bruxelles in Belgium. This 55-kb ele-ment carries genes for biphenyl and chlorobi-phenyl degradation (bph operon) and flankinggenes encoding conjugal transfer functions, suchas those specifying mating pair formation andplasmid replication. The Tn4371 flanking mo-tifs also are found in the chromosomes of severalproteobacteria, suggesting a wide distributionof such genomic elements. Genomic islandsthemselves can retain different degrees of hori-zontal mobility, and their patchwork composi-tion suggests an assembly process driven byHGT.

F I G U R E 2

The three major mechanisms of HGT as they occuramong microbes in the environment. Environ-ments where each process has been documentedand considered to affect microbial community fit-ness are depicted.

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Approaches and Best Niches

for Estimating HGT

Transferants, organisms whose genomesare altered by gene transfers regardless ofmechanism, traditionally were detectedby selection against both donor and re-cipient strains. However, this approachfails when the microbial community atlarge is the “recipient.” Recent ap-proaches that rely on the conditionalexpression of phenotypes prove robustwhen used with proteins such as greenfluorescent protein (GFP, Fig. 3). Forinstance, when gfp is repressed by astrong repressor that is present in thedonor chromosome but not among po-tential recipients, transferants can bereadily detected by fluorescence, ac-cording to Sørin Molin and collabora-tors at the Technical University of Den-mark in Lyngby.

When Søren Sørensen and his co-workers at the University of Copenha-gen combined this GFP approach withflow cytometry to search recipient com-munities for rare fluorescent transcon-jugants, they found 20- to 100-foldhigher conjugal transfer rates of an IncP1 plasmid compared to when they es-timated rates by selective plating. Fur-thermore, when transconjugants wereidentified following fluorescence-acti-vated cell sorting, the Inc P1 plasmidthat was thought to be limited to gram-negative bacteria was found also ingram-positive actinobacteria.

Examining cells from natural com-munities that are subject to HGT byconfocal scanning laser microscopyhelps to show how biofilm architectureand other cellular activities affecttransconjugant populations (Fig. 3).However, although extremely raretransfer events in complex bacterialcommunities might well be the norm innatural environments, those events canbe detected only when transferant popu-lations become dominant.

Some microbial ecologists are exam-ining how nutrient availability, temperature, sa-linity, soil composition, and other factors influ-ence rates of conjugation, transduction, and

transformation. Their results suggest that envi-ronments characterized by high bacterial den-sity, energy, and diversity support HGT. Such

F I G U R E 3

Use of conditional GFP expression to facilitate on-line and single-cell resolved detectionof HGT. A schematic of the approach is shown in panel A, where expression of theplasmid-encoded gfp/rfp is repressed in the donor cell. Upon transfer of the plasmid toa recipient that does not carry lacI in its chromosome, gfp/rfp is expressed and thetransconjugant strain is distinguished by its fluorescence. The right panel shows theapplication to study conjugal plasmid transfer in biofilms. Panels B and C showcomposite x-y projections at different resolutions of x-y image stacks acquired usingconfocal scanning laser microscopy. Shown to the right and below are vertical sectionsthrough the biofilm collected at position indicated by the white arrows. Spatial distribu-tion of green-fluorescent transconjugants (green or yellow) is revealed relative toplasmidless P. putida RI and Acinetobacter sp. strain C6 recipient cells in a model biofilm.The organisms P. putida (red) and Acinetobacter sp. strain C6 (purple) were identified by16S rRNA targeted in situ hybridization. After hybridization, green-fluorescent transcon-jugants appear as either yellow or green, depending on the ratio between the green Gfpsignal and the red hybridization signal. The micrographs suggest that transconjugants arepredominantly found at the periphery of biofilm structures, where contact with donorsmay be highest and growth conditions most favorable (from Bjarke B. Christensen et al.Appl. Environ. Microbiol. 64:2247–2255, 1998).

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environments include interfaces between thesolid, liquid, or gaseous phases, as well as theexternal and internal surfaces of plants and an-imals.

Why and Where Does HGT Matter?

HGT in microbial communities can affect hu-man and environmental health and productiv-ity. In terms of public health, HGT shapes theevolution of pathogens that resist the immunesystem and antibiotic treatments. For example,Anne Summers and colleagues at the Universityof Georgia found that class 1 antibiotic resistanceintegrons, previously thought limited to the Enter-obacteriaceae, are widely distributed among

gram-positive bacteria in poultry litter.This finding raises the possibility thatdrug resistance and pathogenic traits per-sist and may be distributed among indig-enous microbes, even though pathogensmay not survive.

Rampant transfers of antibiotic resis-tance traits among members of microbialcommunities led some researchers to sug-gest that HGT is an adaptive responseinduced by exposure to antibiotics. Atleast in one case, tetracycline can stimu-late the transfer of conjugative and mobi-lized transposons that specify tetracyclineresistance in Bacteroides spp., accordingto Abigail Salyers at the University ofIllinois and her collaborators. The gener-ality of this mechanism is not known.

Meanwhile, other microbial ecolo-gists are seeking to manage contami-nated environments by transferring cat-abolic genes among resident microbialcommunities. For example, Eva Topand her collaborators at Ghent Univer-sity, now at the University of Idaho,seeded soils with Pseudomonas putidacarrying the 2,4-D degradation plasmidpJP4 and showed extensive transfer of theplasmid and a complete degradation ofadded 2,4-D in 19 days, whereas in un-seeded soils the herbicide was stable foras long as 89 days. This approach is in-spired by the occurrence of modular cat-abolic operons in nature.

Jan Roelof van der Meer, now at theUniversite de Lausanne in Switzerland,and collaborators describe the “natural

history” of such recent HGT events in bacterialisolates from a contaminated environment. Abacterial strain with a clc genomic island encod-ing enzymes that degrade chlorocatechols andchlorobenzoate had acquired a gene cluster en-coding an aromatic ring dioxygenase/dehydro-genase, which was found in other bacterialstrains from the same environment. The result-ing strain contains a functional chlorobenzenecatabolic pathway (Fig. 4). The clc island, fur-thermore, readily disseminates via HGT fromPseudomonas sp. B13.

Open Questions To Be Addressed

The microbial gene pool is dynamic, and HGTis an important force in microbial evolution.

F I G U R E 4

Vertical expansion of a catabolic pathway through horizontal gene transfer. Left panel:Chlorobenzoates and chlorocatechols can be efficiently metabolized by microorganisms(e.g., via clc operons) that, however, cannot initiate transformation of chlorobenzenes.Middle panel: Chlorobenzenes can be attacked but not efficiently degraded by microor-ganism that carry the typical aromatic ring dioxygenase-meta cleavage pathway (e.g., viamcb, tod, xyl operons) because chlorocatechol dioxygenation would lead to toxicintermediates. Right panel: By transferring of the chlorocatechol gene cluster, a newproductive pathway is created that permits growth on chlorobenzenes.

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However, little is known about how selec-tively advantageous is gene swapping itselfand how HGT affects accessory genes, eventhough they seem likely to be involved whenmicrobial communities are adapting to chang-ing environments. Moreover, less is knownabout the role of “ORFan genes,” which oftenare linked to these accessory genes.

Insights into these questions will be forthcom-ing as we better characterize the mobilome andlearn more about how environmental condi-tions affect its composition and dynamics. Mi-

crobial communities appear to be awash withmobile elements, and many are likely to befound in still-uncharacterized genomes. Al-though innovative approaches are enabling re-searchers to detect HGT in undisrupted micro-bial communities, they need to move towardspredicting HGT. Doing so will require them todevelop a strong quantitative framework andmodels for calculating HGT rates when interro-gating microbial communities. They also needto determine the role of selection and fitness costin maintaining the mobilome.

ACKNOWLEDGMENTS

Thanks are due to the NSF (BES, MO/MIP) and DOE (NABIR) for support of the June 2004 workshop and research on HGTin the authors’ laboratories. In addition, the contributions of all workshop participants are acknowledged. Thanks areextended to the following for their feedback on thoughts, ideas, and figures for this article: J. P. Gogarten, S. Molin, P. Sobecky,E. Top, J. R. van der Meer, and finally to B. Brejl for figure preparation.

SUGGESTED READING

Breitbart, M., P. Salamon, B. Andresen, J. M. Mahaffy, A. M. Segall, D. Mead, F. Azam, and F. Rohwer. 2002. Genomicanalysis of uncultured marine viral communities. Proc. Natl. Acad. Sci. USA 99:14250–14255.Christensen, B. B., C. Sternberg, J. B. Andersen, L. Eberl, S. Møller, M. Givskov, and S. Molin. 1998. Establishment of newgenetic traits in a microbial biofilm community. Appl. Environ. Microbiol. 64:2247–2255.Dejonghe, W., J. Goris, S. El Fantroussi, M. Hofte, P. De Vos, W. Verstraete, and E. M. Top. 2000. Effect of disseminationof 2,4-dichlorophenoxyacetic acid (2,4-D) degradation plasmids on 2,4-D degradation and on bacterial community structurein two different soil horizons. Appl. Environ. Microbiol. 66:3297–3304.Eisen, J. A. 2000. Horizontal gene transfer among microbial genomes: new insights from complete genome analysis. Curr.Opin. Genet. Dev. 10:606–611.Gogarten, P. J., and J. P. Townsend. Horizontal gene transfer, evolution, and genome innovation. Nature Rev. Microbiol., inpress.Jain, R., M. C. Rivera, and J. A. Lake. 1999. Horizontal gene transfer among genomes: the complexity hypothesis. Proc. Natl.Acad. Sci. USA 96:3801–3806.Lawrence, J. G., and H. Hendrickson. 2003. Lateral gene transfer: when will adolescence end? Mol. Microbiol. 50:739–749.Nandi, S., J. J. Maurer, C. Hofacre, and A. O. Summers. 2004. Gram-positive bacteria are a major reservoir of Class 1antibiotic resistance integrons in poultry litter. Proc. Natl. Acad. Sci. USA 101:7118–7122.Springael, D., and E. M. Top. 2004. Horizontal gene transfer and microbial adaptation to xenobiotics: new types of mobilegenetic elements and lessons from ecological studies. Trends Microbiol. 12:53–58.van der Meer, J. R., and V. Sentchilo. 2003. Genomic islands and the evolution of catabolic pathways in bacteria. Curr. Opin.Biotechnol. 14:248–54.

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