1887

Microbial Genomics logo

Volume 9, Issue 5

Independent origins and evolution of the secondary replicons of the class Gammaproteobacteria Open Access

Abstract

Multipartite genomes, consisting of more than one replicon, have been found in approximately 10 % of bacteria, many of which belong to the phylum Proteobacteria. Many aspects of their origin and evolution, and the possible advantages related to this type of genome structure, remain to be elucidated. Here, we performed a systematic analysis of the presence and distribution of multipartite genomes in the class Gammaproteobacteria, which includes several genera with diverse lifestyles. Within this class, multipartite genomes are mainly found in the order Alteromonadales (mostly in the genus ) and in the family . Our data suggest that the emergence of secondary replicons in Gammaproteobacteria is rare and that they derive from plasmids. Despite their multiple origins, we highlighted the presence of evolutionary trends such as the inverse proportionality of the genome to chromosome size ratio, which appears to be a general feature of bacteria with multipartite genomes irrespective of taxonomic group. We also highlighted some functional trends. The core gene set of the secondary replicons is extremely small, probably limited to essential genes or genes that favour their maintenance in the genome, while the other genes are less conserved. This hypothesis agrees with the idea that the primary advantage of secondary replicons could be to facilitate gene acquisition through horizontal gene transfer, resulting in replicons enriched in genes associated with adaptation to different ecological niches. Indeed, secondary replicons are enriched both in genes that could promote adaptation to harsh environments, such as those involved in antibiotic, biocide and metal resistance, and in functional categories related to the exploitation of environmental resources (e.g. carbohydrates), which can complement chromosomal functions.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): chromid , Gammaproteobacteria , multipartite genomes , Pseudoalteromonas , secondary replicons and Vibrionaceae
Funding
This study was supported by the:
  • PNRA (Piano Nazionale di Ricerca in Antartide) (Award PNRA18_00075)
    • Principle Award Recipient: ElenaPerrin
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001025
2023-05-15
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/mgen/9/5/mgen001025.html?itemId=/content/journal/mgen/10.1099/mgen.0.001025&mimeType=html&fmt=ahah

References

  1. diCenzo GC, Finan TM. The divided bacterial genome: structure, function, and evolution. Microbiol Mol Biol Rev 2017; 81:e00019-17 [View Article] [PubMed]
     [Google Scholar]
  2. diCenzo GC, Mengoni A, Perrin E. Chromids aid genome expansion and functional diversification in the family Burkholderiaceae. Mol Biol Evol 2019; 36:562–574 [View Article] [PubMed]
     [Google Scholar]
  3. Sonnenberg CB, Kahlke T, Haugen P. Vibrionaceae core, shell and cloud genes are non-randomly distributed on Chr 1: an hypothesis that links the genomic location of genes with their intracellular placement. BMC Genomics 2020; 21:695 [View Article] [PubMed]
     [Google Scholar]
  4. Harrison PW, Lower RPJ, Kim NKD, Young JPW. Introducing the bacterial “chromid”: not a chromosome, not a plasmid. Trends Microbiol 2010; 18:141–148 [View Article] [PubMed]
     [Google Scholar]
  5. Heidelberg JF, Eisen JA, Nelson WC, Clayton RA, Gwinn ML et al. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 2000; 406:477–483 [View Article] [PubMed]
     [Google Scholar]
  6. Sonnenberg CB, Haugen P. The Pseudoalteromonas multipartite genome: distribution and expression of pangene categories, and a hypothesis for the origin and evolution of the chromid. G3 2021; 11:jkab256 [View Article] [PubMed]
     [Google Scholar]
  7. Sozhamannan S, Waldminghaus T. Exception to the exception rule: synthetic and naturally occurring single chromosome Vibrio cholerae. Environ Microbiol 2020; 22:4123–4132 [View Article] [PubMed]
     [Google Scholar]
  8. Fournes F, Niault T, Czarnecki J, Tissier-Visconti A, Mazel D et al. The coordinated replication of Vibrio cholerae’s two chromosomes required the acquisition of a unique domain by the RctB initiator. Nucleic Acids Res 2021; 49:11119–11133 [View Article] [PubMed]
     [Google Scholar]
  9. Dikow RB, Smith WL. Genome-level homology and phylogeny of Vibrionaceae (Gammaproteobacteria: Vibrionales) with three new complete genome sequences. BMC Microbiol 2013; 13:80 [View Article] [PubMed]
     [Google Scholar]
  10. Sampaio A, Silva V, Poeta P, Aonofriesei F. Vibrio spp.: life strategies, ecology, and risks in a changing environment. Diversity 2022; 14:97 [View Article]
     [Google Scholar]
  11. Okada K, Iida T, Kita-Tsukamoto K, Honda T. Vibrios commonly possess two chromosomes. J Bacteriol 2005; 187:752–757 [View Article] [PubMed]
     [Google Scholar]
  12. Farmer JJ. The family Vibrionaceae. In Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E. eds The Prokaryotes: A Handbook on the Biology of Bacteria Volume 6: Proteobacteria: Gamma Subclass New York, NY: Springer; 2006 pp 495–507 [View Article]
     [Google Scholar]
  13. Bartlett DH. Extremophilic Vibrionaceae. In The Biology of Vibrios John Wiley & Sons, Ltd; 2006 pp 156–171 accessed 2 September 2022
     [Google Scholar]
  14. Bosi E, Fondi M, Orlandini V, Perrin E, Maida I et al. The pangenome of (Antarctic) Pseudoalteromonas bacteria: evolutionary and functional insights. BMC Genomics 2017; 18: [View Article]
     [Google Scholar]
  15. Bosi E, Fondi M, Maida I, Perrin E, de Pascale D et al. Genome-scale phylogenetic and DNA composition analyses of Antarctic Pseudoalteromonas bacteria reveal inconsistencies in current taxonomic affiliation. Hydrobiologia 2015; 761:85–95 [View Article]
     [Google Scholar]
  16. Duhaime MB, Wichels A, Sullivan MB. Six Pseudoalteromonas strains isolated from surface waters of Kabeltonne, Offshore Helgoland, North Sea. Genome Announc 2016; 4:e01697-15 [View Article] [PubMed]
     [Google Scholar]
  17. Xie B-B, Rong J-C, Tang B-L, Wang S, Liu G et al. Evolutionary trajectory of the replication mode of bacterial replicons. mBio 2021; 12:e02745-20 [View Article] [PubMed]
     [Google Scholar]
  18. Liao L, Liu C, Zeng Y, Zhao B, Zhang J et al. Multipartite genomes and the sRNome in response to temperature stress of an arctic Pseudoalteromonas fuliginea BSW20308. Environ Microbiol 2019; 21:272–285 [View Article] [PubMed]
     [Google Scholar]
  19. Médigue C, Krin E, Pascal G, Barbe V, Bernsel A et al. Coping with cold: the genome of the versatile marine Antarctica bacterium Pseudoalteromonas haloplanktis TAC125. Genome Res 2005; 15:1325–1335 [View Article] [PubMed]
     [Google Scholar]
  20. Rong J-C, Liu M, Li Y, Sun T-Y, Pang X-H et al. Complete genome sequence of a marine bacterium with two chromosomes, Pseudoalteromonas translucida KMM 520T. Marine Genomics 2016; 26:17–20 [View Article]
     [Google Scholar]
  21. Wu M, Scott AJ. Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2. Bioinformatics 2012; 28:1033–1034 [View Article]
     [Google Scholar]
  22. Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar GA et al. Pfam: The protein families database in 2021. Nucleic Acids Res 2021; 49:D412–D419 [View Article] [PubMed]
     [Google Scholar]
  23. Sr E. A new generation of homology search tools based on probabilistic inference. Genome informatics International Conference on Genome Informatics; 2009 https://pubmed.ncbi.nlm.nih.gov/20180275/ accessed 23 November 2022
  24. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods 2015; 12:59–60 [View Article] [PubMed]
     [Google Scholar]
  25. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
     [Google Scholar]
  26. Dagona AG. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic acids symposium series [Internet]; 1999 https://www.academia.edu/2034992/BioEdit_a_user_friendly_biological_sequence_alignment_editor_and_analysis_program_for_Windows_95_98_NT accessed 23 November 2022
  27. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article] [PubMed]
     [Google Scholar]
  28. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49:W293–W296 [View Article] [PubMed]
     [Google Scholar]
  29. Parks DH, Chuvochina M, Rinke C, Mussig AJ, Chaumeil PA et al. GTDB: an ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy. Nucleic Acids Res 2022; 50:D785–D794 [View Article] [PubMed]
     [Google Scholar]
  30. Mendler K, Chen H, Parks DH, Lobb B, Hug LA et al. AnnoTree: visualization and exploration of a functionally annotated microbial tree of life. Nucleic Acids Res 2019; 47:4442–4448 [View Article] [PubMed]
     [Google Scholar]
  31. Callaghan MM, Koch B, Hackett KT, Klimowicz AK, Schaub RE et al. Expression, localization, and protein interactions of the partitioning proteins in the gonococcal type IV secretion system. Front Microbiol 2021; 12:784483 [View Article] [PubMed]
     [Google Scholar]
  32. Alcock BP, Raphenya AR, Lau TTY, Tsang KK, Bouchard M et al. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 2020; 48:D517–D525 [View Article] [PubMed]
     [Google Scholar]
  33. Pal C, Bengtsson-Palme J, Rensing C, Kristiansson E, Larsson DGJ. BacMet: antibacterial biocide and metal resistance genes database. Nucleic Acids Res 2014; 42:D737–43 [View Article] [PubMed]
     [Google Scholar]
  34. Buchfink B, Reuter K, Drost HG. Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat Methods 2021; 18:366–368 [View Article] [PubMed]
     [Google Scholar]
  35. Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006; 22:1658–1659 [View Article] [PubMed]
     [Google Scholar]
  36. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article]
     [Google Scholar]
  37. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article] [PubMed]
     [Google Scholar]
  38. Cantalapiedra CP, Hernández-Plaza A, Letunic I, Bork P, Huerta-Cepas J. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol 2021; 38:5825–5829 [View Article] [PubMed]
     [Google Scholar]
  39. Kirkup BC, Chang L, Chang S, Gevers D, Polz MF. Vibrio chromosomes share common history. BMC Microbiol 2010; 10:137 [View Article] [PubMed]
     [Google Scholar]
  40. Cameron DE, Urbach JM, Mekalanos JJ. A defined transposon mutant library and its use in identifying motility genes in Vibrio cholerae. Proc Natl Acad Sci 2008; 105:8736–8741 [View Article] [PubMed]
     [Google Scholar]
  41. Chao MC, Pritchard JR, Zhang YJ, Rubin EJ, Livny J et al. High-resolution definition of the Vibrio cholerae essential gene set with hidden Markov model–based analyses of transposon-insertion sequencing data. Nucleic Acids Res 2013; 41:9033–9048 [View Article]
     [Google Scholar]
  42. Hubbard TP, Chao MC, Abel S, Blondel CJ, Abel Zur Wiesch P et al. Genetic analysis of Vibrio parahaemolyticus intestinal colonization. Proc Natl Acad Sci 2016; 113:6283–6288 [View Article] [PubMed]
     [Google Scholar]
  43. Bekaert M, Goffin N, McMillan S, Desbois AP. Essential genes of Vibrio anguillarum and other Vibrio spp. guide the development of new drugs and vaccines. Front Microbiol 2021; 12:755801 [View Article]
     [Google Scholar]
  44. Hall JPJ, Botelho J, Cazares A, Baltrus DA. What makes a megaplasmid?. Philos Trans R Soc Lond B Biol Sci 2022; 377:20200472 [View Article] [PubMed]
     [Google Scholar]
  45. Vieira-Silva S, Touchon M, Rocha EPC. No evidence for elemental-based streamlining of prokaryotic genomes. Trends Ecol Evol 2010; 25:319–320 [View Article] [PubMed]
     [Google Scholar]
  46. MacLean AM, Finan TM, Sadowsky MJ. Genomes of the symbiotic nitrogen-fixing bacteria of legumes. Plant Physiol 2007; 144:615–622 [View Article] [PubMed]
     [Google Scholar]
  47. Harrison E, Brockhurst MA. Plasmid-mediated horizontal gene transfer is a coevolutionary process. Trends Microbiol 2012; 20:262–267 [View Article] [PubMed]
     [Google Scholar]
  48. Brockhurst MA, Harrison E. Ecological and evolutionary solutions to the plasmid paradox. Trends Microbiol 2022; 30:534–543 [View Article] [PubMed]
     [Google Scholar]
  49. Higgins S, Sanchez-Contreras M, Gualdi S, Pinto-Carbó M, Carlier A et al. The essential genome of Burkholderia cenocepacia H111. J Bacteriol 2017; 199:e00260-17 [View Article] [PubMed]
     [Google Scholar]
  50. diCenzo GC, Benedict AB, Fondi M, Walker GC, Finan TM et al. Robustness encoded across essential and accessory replicons of the ecologically versatile bacterium Sinorhizobium meliloti. PLOS Genet 2018; 14:e1007357 [View Article]
     [Google Scholar]
  51. diCenzo GC, Checcucci A, Bazzicalupo M, Mengoni A, Viti C et al. Metabolic modelling reveals the specialization of secondary replicons for niche adaptation in Sinorhizobium meliloti. Nat Commun 2016; 7:12219 [View Article] [PubMed]
     [Google Scholar]
  52. Agnoli K, Schwager S, Uehlinger S, Vergunst A, Viteri DF et al. Exposing the third chromosome of Burkholderia cepacia complex strains as a virulence plasmid. Mol Microbiol 2012; 83:362–378 [View Article] [PubMed]
     [Google Scholar]
  53. Agnoli K, Frauenknecht C, Freitag R, Schwager S, Jenul C et al. The third replicon of members of the Burkholderia cepacia complex, plasmid pC3, plays a role in stress tolerance. Appl Environ Microbiol 2014; 80:1340–1348 [View Article] [PubMed]
     [Google Scholar]
  54. Fagorzi C, Bacci G, Huang R, Cangioli L, Checcucci A et al. Nonadditive transcriptomic signatures of genotype-by-genotype interactions during the initiation of plant-rhizobium symbiosis. mSystems 2021; 6:e00974-20 [View Article] [PubMed]
     [Google Scholar]
  55. diCenzo GC, MacLean AM, Milunovic B, Golding GB, Finan TM. Examination of prokaryotic multipartite genome evolution through experimental genome reduction. PLoS Genet 2014; 10:e1004742 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.001025
Loading
Independent origins and evolution of the secondary replicons of the class Gammaproteobacteria
M Gen 9, 001025 (2023); https://doi.org/10.1099/mgen.0.001025
/content/journal/mgen/10.1099/mgen.0.001025
/content/journal/mgen/10.1099/mgen.0.001025
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error