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Genomic erosion and extensive horizontal gene transfer in gut-associated Acetobacteraceae.

Publication ,  Journal Article
Brown, BP; Wernegreen, JJ
Published in: BMC genomics
June 2019

Symbiotic relationships between animals and bacteria have profound impacts on the evolutionary trajectories of each partner. Animals and gut bacteria engage in a variety of relationships, occasionally persisting over evolutionary timescales. Ants are a diverse group of animals that engage in many types of associations with taxonomically distinct groups of bacterial associates. Here, we bring into culture and characterize two closely-related strains of gut associated Acetobacteraceae (AAB) of the red carpenter ant, Camponotus chromaiodes.Genome sequencing, assembly, and annotation of both strains delineate stark patterns of genomic erosion and sequence divergence in gut associated AAB. We found widespread horizontal gene transfer (HGT) in these bacterial associates and report elevated gene acquisition associated with energy production and conversion, amino acid and coenzyme transport and metabolism, defense mechanisms, and lysine export. Both strains have acquired the complete NADH-quinone oxidoreductase complex, plausibly from an Enterobacteriaceae origin, likely facilitating energy production under diverse conditions. Conservation of several lysine biosynthetic and salvage pathways and accumulation of lysine export genes via HGT implicate L-lysine supplementation by both strains as a potential functional benefit for the host. These trends are contrasted by genome-wide erosion of several amino acid biosynthetic pathways and pathways in central metabolism. We perform phylogenomic analyses on both strains as well as several free living and host associated AAB. Based on their monophyly and deep divergence from other AAB, these C. chromaiodes gut associates may represent a novel genus. Together, our results demonstrate how extensive horizontal transfer between gut associates along with genome-wide deletions leads to mosaic metabolic pathways. More broadly, these patterns demonstrate that HGT and genomic erosion shape metabolic capabilities of persistent gut associates and influence their genomic evolution.Using comparative genomics, our study reveals substantial changes in genomic content in persistent associates of the insect gastrointestinal tract and provides evidence for the evolutionary pressures inherent to this environment. We describe patterns of genomic erosion and horizontal acquisition that result in mosaic metabolic pathways. Accordingly, the phylogenetic position of both strains of these associates form a divergent, monophyletic clade sister to gut associates of honey bees and more distantly to Gluconobacter.

Duke Scholars

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Published In

BMC genomics

DOI

EISSN

1471-2164

ISSN

1471-2164

Publication Date

June 2019

Volume

20

Issue

1

Start / End Page

472

Related Subject Headings

  • Symbiosis
  • Phylogeny
  • Metabolic Networks and Pathways
  • Genomics
  • Gene Transfer, Horizontal
  • Gastrointestinal Tract
  • Evolution, Molecular
  • Bioinformatics
  • Ants
  • Animals
 

Citation

APA
Chicago
ICMJE
MLA
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Brown, B. P., & Wernegreen, J. J. (2019). Genomic erosion and extensive horizontal gene transfer in gut-associated Acetobacteraceae. BMC Genomics, 20(1), 472. https://doi.org/10.1186/s12864-019-5844-5
Brown, Bryan P., and Jennifer J. Wernegreen. “Genomic erosion and extensive horizontal gene transfer in gut-associated Acetobacteraceae.BMC Genomics 20, no. 1 (June 2019): 472. https://doi.org/10.1186/s12864-019-5844-5.
Brown, Bryan P., and Jennifer J. Wernegreen. “Genomic erosion and extensive horizontal gene transfer in gut-associated Acetobacteraceae.BMC Genomics, vol. 20, no. 1, June 2019, p. 472. Epmc, doi:10.1186/s12864-019-5844-5.
Journal cover image

Published In

BMC genomics

DOI

EISSN

1471-2164

ISSN

1471-2164

Publication Date

June 2019

Volume

20

Issue

1

Start / End Page

472

Related Subject Headings

  • Symbiosis
  • Phylogeny
  • Metabolic Networks and Pathways
  • Genomics
  • Gene Transfer, Horizontal
  • Gastrointestinal Tract
  • Evolution, Molecular
  • Bioinformatics
  • Ants
  • Animals