Host range diversification within the IncP-1 plasmid group

Yano, Hirokazu; Rogers, Linda; Knox, Molly G.; Heuer, Holger; Smalla, Kornelia; Brown, Celeste J.; Top, Eva M.

doi:10.1099/mic.0.068387-0

Cited by 32 publications

(41 citation statements)

References 76 publications

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“…Therefore, the majority of transconjugant OTUs were only identified in single donorplasmid combinations. This might result from mating pair combinations that each favor or reduce gene transfer abilities (Bingle et al, 2003;Thomas and Nielsen, 2005;Yano et al, 2013).…”

Section: Resultsmentioning

confidence: 99%

“…Yano et al (2013) hypothesized that genetic differences appearing among closely related IncP-1 plasmids through plasmid backbone evolution can result in significant diversities in host range efficiency without affecting their broad host range nature. Such backbone alterations exist between the IncP-1a (RP4) and IncP-1e (pKJK5) core regulatory proteins such as KorB, TrfA, TrbA and Ssb (Bahl et al, 2007).…”

Section: Resultsmentioning

confidence: 99%

“…class 1 integron of pKJK5) delivering packages of fitness altering DNA without the need for plasmid replication. Additionally, transient hosts can increase the transfer range further by allowing transfer to organisms that had a lower transfer potential from the original donor strain (Yano et al, 2013).…”

Section: Ecological and Evolutionary Relevancementioning

confidence: 99%

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Broad host range plasmids can invade an unexpectedly diverse fraction of a soil bacterial community

et al. 2014

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Conjugal plasmids can provide microbes with full complements of new genes and constitute potent vehicles for horizontal gene transfer. Conjugal plasmid transfer is deemed responsible for the rapid spread of antibiotic resistance among microbes. While broad host range plasmids are known to transfer to diverse hosts in pure culture, the extent of their ability to transfer in the complex bacterial communities present in most habitats has not been comprehensively studied. Here, we isolated and characterized transconjugants with a degree of sensitivity not previously realized to investigate the transfer range of IncP-and IncPromA-type broad host range plasmids from three proteobacterial donors to a soil bacterial community. We identified transfer to many different recipients belonging to 11 different bacterial phyla. The prevalence of transconjugants belonging to diverse Gram-positive Firmicutes and Actinobacteria suggests that inter-Gram plasmid transfer of IncP-1 and IncPromAtype plasmids is a frequent phenomenon. While the plasmid receiving fractions of the community were both plasmid-and donor-dependent, we identified a core super-permissive fraction that could take up different plasmids from diverse donor strains. This fraction, comprising 80% of the identified transconjugants, thus has the potential to dominate IncP-and IncPromA-type plasmid transfer in soil. Our results demonstrate that these broad host range plasmids have a hitherto unrecognized potential to transfer readily to very diverse bacteria and can, therefore, directly connect large proportions of the soil bacterial gene pool. This finding reinforces the evolutionary and medical significances of these plasmids.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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Broad host range plasmids can invade an unexpectedly diverse fraction of a soil bacterial community

et al. 2014

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“…Plasmid pMBUI1 belongs to the IncP-1␥ subgroup (45) and is closely related to the archetype pQKH54 (46). Its characteristics are described elsewhere (47). Plasmid pMBUI3 (Fig.…”

Section: Resultsmentioning

confidence: 99%

Diverse Broad-Host-Range Plasmids from Freshwater Carry Few Accessory Genes

Brown

Sen

Yano

et al. 2013

Appl Environ Microbiol

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c Broad-host-range self-transferable plasmids are known to facilitate bacterial adaptation by spreading genes between phylogenetically distinct hosts. These plasmids typically have a conserved backbone region and a variable accessory region that encodes host-beneficial traits. We do not know, however, how well plasmids that do not encode accessory functions can survive in nature. The goal of this study was to characterize the backbone and accessory gene content of plasmids that were captured from freshwater sources without selecting for a particular phenotype or cultivating their host. To do this, triparental matings were used such that the only required phenotype was the plasmid's ability to mobilize a nonconjugative plasmid. Based on complete genome sequences of 10 plasmids, only 5 carried identifiable accessory gene regions, and none carried antibiotic resistance genes. The plasmids belong to four known incompatibility groups (IncN, IncP-1, IncU, and IncW) and two potentially new groups. Eight of the plasmids were shown to have a broad host range, being able to transfer into alpha-, beta-, and gammaproteobacteria. Because of the absence of antibiotic resistance genes, we resampled one of the sites and compared the proportion of captured plasmids that conferred antibiotic resistance to their hosts with the proportion of such plasmids captured from the effluent of a local wastewater treatment plant. Few of the captured plasmids from either site encoded antibiotic resistance. A high diversity of plasmids that encode no or unknown accessory functions is thus readily found in freshwater habitats. The question remains how the plasmids persist in these microbial communities.

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“…Potential plasmid recipients can stretch across diverse microbial groups (13), and although transconjugants within sink species may be transient (due to segregation or purifying selection) (28), their continual replenishment by conjugation from the source means that microbial community richness may be more robust to occasional bouts of selection for plasmid-borne genes. Coculture enhanced plasmid persistence in the sink species even under Hg(II) selection, whereas in single-species P. putida cultures, plasmid carriers tended to be outcompeted by mutants with chromosomal Hg R .…”

Section: Discussionmentioning

confidence: 99%

Source–sink plasmid transfer dynamics maintain gene mobility in soil bacterial communities

Hall

Wood

Harrison

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

169

230

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Horizontal gene transfer is a fundamental process in bacterial evolution that can accelerate adaptation via the sharing of genes between lineages. Conjugative plasmids are the principal genetic elements mediating the horizontal transfer of genes, both within and between bacterial species. In some species, plasmids are unstable and likely to be lost through purifying selection, but when alternative hosts are available, interspecific plasmid transfer could counteract this and maintain access to plasmid-borne genes. To investigate the evolutionary importance of alternative hosts to plasmid population dynamics in an ecologically relevant environment, we established simple soil microcosm communities comprising two species of common soil bacteria, Pseudomonas fluorescens and Pseudomonas putida, and a mercury resistance (Hg R ) plasmid, pQBR57, both with and without positive selection [i.e., addition of Hg(II)]. In single-species populations, plasmid stability varied between species: although pQBR57 survived both with and without positive selection in P. fluorescens, it was lost or replaced by nontransferable Hg R captured to the chromosome in P. putida. A simple mathematical model suggests these differences were likely due to pQBR57's lower intraspecific conjugation rate in P. putida. By contrast, in two-species communities, both models and experiments show that interspecific conjugation from P. fluorescens allowed pQBR57 to persist in P. putida via source-sink transfer dynamics. Moreover, the replacement of pQBR57 by nontransferable chromosomal Hg R in P. putida was slowed in coculture. Interspecific transfer allows plasmid survival in host species unable to sustain the plasmid in monoculture, promoting community-wide access to the plasmid-borne accessory gene pool and thus potentiating future evolvability.horizontal gene transfer | plasmids | mobile genetic elements | microbial ecology

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Host range diversification within the IncP-1 plasmid group

Cited by 32 publications

References 76 publications

Broad host range plasmids can invade an unexpectedly diverse fraction of a soil bacterial community

Broad host range plasmids can invade an unexpectedly diverse fraction of a soil bacterial community

Diverse Broad-Host-Range Plasmids from Freshwater Carry Few Accessory Genes

Source–sink plasmid transfer dynamics maintain gene mobility in soil bacterial communities

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