Abstract
Intraspecies diversification and niche adaptation by members of the Vibrio genus, one of the most diverse bacterial genera, is thought to be driven by horizontal gene transfer. However, the intrinsic driving force of Vibrio species diversification is much less explored. Here, by studying two dominant and competing cohabitants of the gastric cavity of corals, we found that a phenotype influencing island (named VPII) in Vibrio alginolyticus was eliminated upon coculturing with Pseudoalteromonas. The loss of VPII reduced the biofilm formation and phage resistance, but activated motility, which may allow V. alginolyticus to expand to other niches. Mechanistically, we discovered that the excision of this island is mediated by the cooperation of two unrelated mobile genetic elements harbored in Pseudoalteromonas spp., an integrative and conjugative element (ICE) and a mobilizable genomic island (MGI). More importantly, these mobile genetic elements are widespread in cohabitating Gram-negative bacteria. Altogether, we discovered a new strategy by which the mobilome is employed by competitors to increase the genomic plasticity of rivals.
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Data availability
The complete genome sequences of the strains Va43097, Ps43088, Ps43101, Ps43095, and phage vB_ValP-FGH have been deposited in GenBank under the accession numbers CP071840-CP071841, CP072675-CP072676, CP072673-CP072674, CP087995-CP087996, and OL762410. The transcriptome data of Va43097 and its variants can be freely accessed via the Science Data Bank at https://doi.org/10.57760/sciencedb.01844.
References
Reen FJ, Almagro-Moreno S, Ussery D, Boyd EF. The genomic code: inferring Vibrionaceae niche specialization. Nat Rev Microbiol. 2006;4:697–704.
Thompson FL, Iida T, Swings J. Biodiversity of vibrios. Microbiol Mol Biol Rev. 2004;68:403–31.
Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I. The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol. 2007;5:355–62.
Neulinger SC, Jarnegren J, Ludvigsen M, Lochte K, Dullo WC. Phenotype-specific bacterial communities in the cold-water coral Lophelia pertusa (Scleractinia) and their implications for the coral’s nutrition, health, and distribution. Appl Environ Microbiol. 2008;74:7272–85.
Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N. Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs. 2001;20:85–91.
Huang JF, Wu RB, Liu D, Liao BQ, Lei M, Wang M, et al. Mechanistic insight into the binding and swelling functions of prepeptidase C-terminal (PPC) domains from various bacterial proteases. Appl Environ Microbiol. 2019;85:e00611-19.
Paulsen SS, Strube ML, Bech PK, Gram L, Sonnenschein EC. Marine chitinolytic Pseudoalteromonas represents an untapped reservoir of bioactive potential. Msystems. 2019;4:e00060-19.
Lv XR, Li Y, Cui TQ, Sun MT, Bai FL, Li XP, et al. Bacterial community succession and volatile compound changes during fermentation of shrimp paste from Chinese Jinzhou region. Lwt-Food Sci Technol. 2020;122:108998.
Richards GP, Watson MA, Needleman DS, Uknalis J, Boyd EF, Fay JP. Mechanisms for Pseudoalteromonas piscicida-induced killing of Vibrios and other bacterial pathogens. Appl Environ Microbiol. 2017;83:e00175-17.
Bernbom N, Ng YY, Kjelleberg S, Harder T, Gram L. Marine bacteria from Danish coastal waters show antifouling activity against the marine fouling bacterium Pseudoalteromonas sp. strain S91 and zoospores of the green alga Ulva australis independent of bacteriocidal activity. Appl Environ Microbiol. 2011;77:8557–67.
Muras A, Parga A, Mayer C, Otero A. Use of quorum sensing inhibition strategies to control microfouling. Mar Drugs. 2021;19:14.
Shnit-Orland M, Kushmaro A. Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol Ecol. 2009;67:371–80.
Rosado PM, Leite DCA, Duarte GAS, Chaloub RM, Jospin G, Nunes da Rocha U, et al. Marine probiotics: increasing coral resistance to bleaching through microbiome manipulation. ISME J. 2019;13:921–36.
Wang P, Yu Z, Li B, Cai X, Zeng Z, Chen X, et al. Development of an efficient conjugation-based genetic manipulation system for Pseudoalteromonas. Micro Cell Fact. 2015;14:11.
Wang P, He D, Li B, Guo Y, Wang W, Luo X, et al. Eliminating mcr-1-harbouring plasmids in clinical isolates using the CRISPR/Cas9 system. J Antimicrob Chemother. 2019;74:2559–65.
Wang P, Zeng Z, Wang W, Wen Z, Li J, Wang X. Dissemination and loss of a biofilm-related genomic island in marine Pseudoalteromonas mediated by integrative and conjugative elements. Environ Microbiol. 2017;19:4620–37.
Zeng Z, Liu X, Yao J, Guo Y, Li B, Li Y, et al. Cold adaptation regulated by cryptic prophage excision in Shewanella oneidensis. ISME J 2016;10:2787–800.
Miller JH. Experiments in molecular genetics. Cold Spring Harbor. NY: Cold Spring Harbor Laboratory Press; 1972.
Bertani LE, Bertani G. Preparation and characterization of temperate, non-inducible bacteriophage P2 (host: Escherichia coli). J Gen Virol. 1970;6:201–12.
Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, et al. The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res. 2014;42:D206–D14.
Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S. Biofilms: an emergent form of bacterial life. Nat Rev Microbiol. 2016;14:563–75.
Dang H, Lovell CR. Microbial surface colonization and biofilm development in marine environments. Microbiol Mol Biol Rev. 2016;80:91–138.
Baker-Austin C, Oliver JD, Alam M, Ali A, Waldor MK, Qadri F, et al. Vibrio spp. infections. Nat Rev Dis Prim. 2018;4:8.
Iijima S, Washio K, Okahara R, Morikawa M. Biofilm formation and proteolytic activities of Pseudoalteromonas bacteria that were isolated from fish farm sediments. Micro Biotechnol. 2009;2:361–9.
Kimbrough JH, McCarter LL. Identification of three new GGDEF and EAL domain-containing proteins participating in the Scr surface colonization regulatory network in Vibrio parahaemolyticus. J Bacteriol. 2021;203:e00409-20.
Brenciani A, Bacciaglia A, Vignaroli C, Pugnaloni A, Varaldo PE, Giovanetti E. Phim46.1, the main Streptococcus pyogenes element carrying mef(A) and tet(O) genes. Antimicrob Agents Chemother. 2010;54:221–9.
Breitbart M, Bonnain C, Malki K, Sawaya NA. Phage puppet masters of the marine microbial realm. Nat Microbiol. 2018;3:754–66.
Kropinski AM, Prangishvili D, Lavigne R. Position paper: the creation of a rational scheme for the nomenclature of viruses of Bacteria and Archaea. Environ Microbiol. 2009;11:2775–7.
Ferreira RB, Chodur DM, Antunes LC, Trimble MJ, McCarter LL. Output targets and transcriptional regulation by a cyclic dimeric GMP-responsive circuit in the Vibrio parahaemolyticus Scr network. J Bacteriol. 2012;194:914–24.
Daccord A, Ceccarelli D, Burrus V. Integrating conjugative elements of the SXT/R391 family trigger the excision and drive the mobilization of a new class of Vibrio genomic islands. Mol Microbiol. 2010;78:576–88.
Poulin-Laprade D, Matteau D, Jacques PE, Rodrigue S, Burrus V. Transfer activation of SXT/R391 integrative and conjugative elements: unraveling the SetCD regulon. Nucleic Acids Res. 2015;43:2045–56.
Ghoul M, Mitri S. The ecology and evolution of microbial competition. Trends Microbiol. 2016;24:833–45.
Bauer MA, Kainz K, Carmona-Gutierrez D, Madeo F. Microbial wars: competition in ecological niches and within the microbiome. Micro Cell. 2018;5:215–9.
Yu M, Wang J, Tang K, Shi X, Wang S, Zhu WM, et al. Purification and characterization of antibacterial compounds of Pseudoalteromonas flavipulchra JG1. Microbiology. 2012;158:835–42.
Yawata Y, Cordero OX, Menolascina F, Hehemann JH, Polz MF, Stocker R. Competition-dispersal tradeoff ecologically differentiates recently speciated marine bacterioplankton populations. Proc Natl Acad Sci USA. 2014;111:5622–7.
Ni L, Yang S, Zhang R, Jin Z, Chen H, Conrad JC, et al. Bacteria differently deploy type-IV pili on surfaces to adapt to nutrient availability. NPJ Biofilms Microbiomes. 2016;2:15029.
Jenal U, Malone J. Mechanisms of cyclic-di-GMP signaling in bacteria. Annu Rev Genet. 2006;40:385–407.
Bordeleau E, Brouillette E, Robichaud N, Burrus V. Beyond antibiotic resistance: integrating conjugative elements of the SXT/R391 family that encode novel diguanylate cyclases participate to c-di-GMP signalling in Vibrio cholerae. Environ Microbiol. 2010;12:510–23.
Ha DG, Richman ME, O’Toole GA. Deletion mutant library for investigation of functional outputs of cyclic diguanylate metabolism in Pseudomonas aeruginosa PA14. Appl Environ Microbiol. 2014;80:3384–93.
Juhas M, van der Meer JR, Gaillard M, Harding RM, Hood DW, Crook DW. Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol Rev. 2009;33:376–93.
Dobrindt U, Hochhut B, Hentschel U, Hacker J. Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol. 2004;2:414–24.
Bioteau A, Durand R, Burrus V. Redefinition and unification of the SXT/R391 family of integrative and conjugative elements. Appl Environ Microbiol. 2018;84:e00485-18.
Carr VR, Shkoporov A, Hill C, Mullany P, Moyes DL. Probing the mobilome: discoveries in the dynamic microbiome. Trends Microbiol. 2021;29:158–70.
Acknowledgements
This work was supported by the Local Innovative and Research Teams Project of Guangdong Pearl River Talents Program (2019BT02Y262), the National Natural Science Foundation of China (42188102, 91951203, 31625001 and 32070175), the K. C. Wong Education Foundation (GJTD-2020-12), the Youth Innovation Promotion Association CAS (2021345 to P.W), the Guangdong Major Project of Basic and Applied Basic Research (2019B030302004), the Natural Science Foundation of Guangdong Province (2019A1515011912), the Science and Technology Planning Project of Guangzhou (202002030493) and the Key Special Project for Introduced Talents Team of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (GML2019ZD0407).
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PW and XW designed the study. PW, YZ, and WW performed the experiments. PW and XW analyzed the study. SL, KT, and TL contributed new reagents/analytic tools. PW and XW wrote the paper. TKW helped edit the manuscript. All authors read and approved the final manuscript.
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Wang, P., Zhao, Y., Wang, W. et al. Mobile genetic elements used by competing coral microbial populations increase genomic plasticity. ISME J 16, 2220–2229 (2022). https://doi.org/10.1038/s41396-022-01272-1
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DOI: https://doi.org/10.1038/s41396-022-01272-1
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