Evidence of Extensive DNA Transfer between <italic toggle="yes">Bacteroidales</italic> Species within the Human Gut
ABSTRACT The genome sequences of intestinal Bacteroidales strains reveal evidence of extensive horizontal gene transfer. In vitro studies of Bacteroides and other bacteria have addressed mechanisms of conjugative transfer and some phenotypic outcomes of these DNA acquisitions in the recipient, such...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2014-07-01
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| Series: | mBio |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.01305-14 |
| _version_ | 1818843766866313216 |
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| author | Michael J. Coyne Naamah Levy Zitomersky Abigail Manson McGuire Ashlee M. Earl Laurie E. Comstock |
| author_facet | Michael J. Coyne Naamah Levy Zitomersky Abigail Manson McGuire Ashlee M. Earl Laurie E. Comstock |
| author_sort | Michael J. Coyne |
| collection | DOAJ |
| description | ABSTRACT The genome sequences of intestinal Bacteroidales strains reveal evidence of extensive horizontal gene transfer. In vitro studies of Bacteroides and other bacteria have addressed mechanisms of conjugative transfer and some phenotypic outcomes of these DNA acquisitions in the recipient, such as the acquisition of antibiotic resistance. However, few studies have addressed the horizontal transfer of genetic elements between bacterial species coresident in natural microbial communities, especially microbial ecosystems of humans. Here, we examine the genomes of Bacteroidales species from two human adults to identify genetic elements that were likely transferred among these Bacteroidales while they were coresident in the intestine. Using seven coresident Bacteroidales species from one individual and eight from another, we identified five large chromosomal regions, each present in a minimum of three of the coresident strains at near 100% DNA identity. These five regions are not found in any other sequenced Bacteroidetes genome at this level of identity and are likely all integrative conjugative elements (ICEs). Such highly similar and unique regions occur in only 0.4% of phylogenetically representative mock communities, providing strong evidence that these five regions were transferred between coresident strains in these subjects. In addition to the requisite proteins necessary for transfer, these elements encode proteins predicted to increase fitness, including orphan DNA methylases that may alter gene expression, fimbriae synthesis proteins that may facilitate attachment and the utilization of new substrates, putative secreted antimicrobial molecules, and a predicted type VI secretion system (T6SS), which may confer a competitive ecological advantage to these strains in their complex microbial ecosystem. IMPORTANCE By analyzing Bacteroidales strains coresident in the gut microbiota of two human adults, we provide strong evidence for extensive interspecies and interfamily transfer of integrative conjugative elements within the intestinal microbiota of individual humans. In the recipient strain, we show that the conjugative elements themselves can be modified by the transposition of insertion sequences and retroelements from the recipient’s genome, with subsequent transfer of these modified elements to other members of the microbiota. These data suggest that the genomes of our gut bacteria are substantially modified by other, coresident members of the ecosystem, resulting in highly personalized Bacteroidales strains likely unique to that individual. The genetic content of these ICEs suggests that their transfer from successful adapted members of an ecosystem confers beneficial properties to the recipient, increasing its fitness and allowing it to better compete within its particular personalized gut microbial ecosystem. |
| first_indexed | 2024-12-19T05:03:05Z |
| format | Article |
| id | doaj.art-a3df0e683fff48698a921b423b4af088 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-19T05:03:05Z |
| publishDate | 2014-07-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-a3df0e683fff48698a921b423b4af0882022-12-21T20:35:01ZengAmerican Society for MicrobiologymBio2150-75112014-07-015310.1128/mBio.01305-14Evidence of Extensive DNA Transfer between <italic toggle="yes">Bacteroidales</italic> Species within the Human GutMichael J. Coyne0Naamah Levy Zitomersky1Abigail Manson McGuire2Ashlee M. Earl3Laurie E. Comstock4Division of Infectious Diseases, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts, USADivision of Gastroenterology, Boston Children’s Hospital, Harvard Medical School, Boston, Massachusetts, USABroad Institute, Cambridge, Massachusetts, USABroad Institute, Cambridge, Massachusetts, USADivision of Infectious Diseases, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts, USAABSTRACT The genome sequences of intestinal Bacteroidales strains reveal evidence of extensive horizontal gene transfer. In vitro studies of Bacteroides and other bacteria have addressed mechanisms of conjugative transfer and some phenotypic outcomes of these DNA acquisitions in the recipient, such as the acquisition of antibiotic resistance. However, few studies have addressed the horizontal transfer of genetic elements between bacterial species coresident in natural microbial communities, especially microbial ecosystems of humans. Here, we examine the genomes of Bacteroidales species from two human adults to identify genetic elements that were likely transferred among these Bacteroidales while they were coresident in the intestine. Using seven coresident Bacteroidales species from one individual and eight from another, we identified five large chromosomal regions, each present in a minimum of three of the coresident strains at near 100% DNA identity. These five regions are not found in any other sequenced Bacteroidetes genome at this level of identity and are likely all integrative conjugative elements (ICEs). Such highly similar and unique regions occur in only 0.4% of phylogenetically representative mock communities, providing strong evidence that these five regions were transferred between coresident strains in these subjects. In addition to the requisite proteins necessary for transfer, these elements encode proteins predicted to increase fitness, including orphan DNA methylases that may alter gene expression, fimbriae synthesis proteins that may facilitate attachment and the utilization of new substrates, putative secreted antimicrobial molecules, and a predicted type VI secretion system (T6SS), which may confer a competitive ecological advantage to these strains in their complex microbial ecosystem. IMPORTANCE By analyzing Bacteroidales strains coresident in the gut microbiota of two human adults, we provide strong evidence for extensive interspecies and interfamily transfer of integrative conjugative elements within the intestinal microbiota of individual humans. In the recipient strain, we show that the conjugative elements themselves can be modified by the transposition of insertion sequences and retroelements from the recipient’s genome, with subsequent transfer of these modified elements to other members of the microbiota. These data suggest that the genomes of our gut bacteria are substantially modified by other, coresident members of the ecosystem, resulting in highly personalized Bacteroidales strains likely unique to that individual. The genetic content of these ICEs suggests that their transfer from successful adapted members of an ecosystem confers beneficial properties to the recipient, increasing its fitness and allowing it to better compete within its particular personalized gut microbial ecosystem.https://journals.asm.org/doi/10.1128/mBio.01305-14 |
| spellingShingle | Michael J. Coyne Naamah Levy Zitomersky Abigail Manson McGuire Ashlee M. Earl Laurie E. Comstock Evidence of Extensive DNA Transfer between <italic toggle="yes">Bacteroidales</italic> Species within the Human Gut mBio |
| title | Evidence of Extensive DNA Transfer between <italic toggle="yes">Bacteroidales</italic> Species within the Human Gut |
| title_full | Evidence of Extensive DNA Transfer between <italic toggle="yes">Bacteroidales</italic> Species within the Human Gut |
| title_fullStr | Evidence of Extensive DNA Transfer between <italic toggle="yes">Bacteroidales</italic> Species within the Human Gut |
| title_full_unstemmed | Evidence of Extensive DNA Transfer between <italic toggle="yes">Bacteroidales</italic> Species within the Human Gut |
| title_short | Evidence of Extensive DNA Transfer between <italic toggle="yes">Bacteroidales</italic> Species within the Human Gut |
| title_sort | evidence of extensive dna transfer between italic toggle yes bacteroidales italic species within the human gut |
| url | https://journals.asm.org/doi/10.1128/mBio.01305-14 |
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