1887

Abstract

The roseobacter group of marine bacteria is characterized by a mosaic distribution of ecologically important phenotypes. These are often encoded on mobile extrachromosomal replicons. So far, conjugation had only been experimentally proven between the two model organisms and . Here, we show that two large natural RepABC-type plasmids from can be transferred into representatives of all known major lineages. Complete genome sequencing of the newly established transconjugants confirmed their genomic integrity. The conjugated plasmids were stably maintained as single copy number replicons in the genuine as well as the new host. Co-cultivation of and the transconjugants with the dinoflagellate demonstrated that is a probiotic strain that improves the yield and stability of the dinoflagellate culture. The transconjugant carrying the 191 kb plasmid, but not the 126 kb sister plasmid, killed the dinoflagellate in co-culture.

Funding
This study was supported by the:
  • Deutsche Forschungsgemeinschaft (Award 34509606)
    • Principle Award Recipient: NotApplicable
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000787
2022-03-07
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/mgen/8/3/mgen000787.html?itemId=/content/journal/mgen/10.1099/mgen.0.000787&mimeType=html&fmt=ahah

References

  1. Ambrose SJ, Harmer CJ, Hall RM. Evolution and typing of IncC plasmids contributing to antibiotic resistance in Gram-negative bacteria. Plasmid 2018; 99:40–55 [View Article] [PubMed]
    [Google Scholar]
  2. Partridge SR, Kwong SM, Firth N, Jensen SO. Mobile genetic elements associated with antimicrobial resistance. Clin Microbiol Rev 2018; 31:e00088-17 [View Article] [PubMed]
    [Google Scholar]
  3. San Millan A. Evolution of plasmid-mediated antibiotic resistance in the clinical context. Trends Microbiol 2018; 26:978–985 [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. Petersen J, Frank O, Göker M, Pradella S. Extrachromosomal, extraordinary and essential – the plasmids of the Roseobacter clade. Appl Microbiol Biotechnol 2013; 97:2805–2815 [View Article] [PubMed]
    [Google Scholar]
  6. Simon M, Scheuner C, Meier-Kolthoff JP, Brinkhoff T, Wagner-Döbler I et al. Phylogenomics of Rhodobacteraceae reveals evolutionary adaptation to marine and non-marine habitats. ISME J 2017; 11:1483–1499 [View Article] [PubMed]
    [Google Scholar]
  7. Buchan A, LeCleir GR, Gulvik CA, González JM. Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Microbiol 2014; 12:686–698 [View Article] [PubMed]
    [Google Scholar]
  8. Luo H, Moran MA. Evolutionary ecology of the marine Roseobacter clade. Microbiol Mol Biol Rev 2014; 78:573–587 [View Article] [PubMed]
    [Google Scholar]
  9. Frank O, Göker M, Pradella S, Petersen J. Ocean’s Twelve: flagellar and biofilm chromids in the multipartite genome of Marinovum algicola DG898 exemplify functional compartmentalization. Environ Microbiol 2015; 17:4019–4034 [View Article] [PubMed]
    [Google Scholar]
  10. Petersen J, Vollmers J, Ringel V, Brinkmann H, Ellebrandt-Sperling C et al. A marine plasmid hitchhiking vast phylogenetic and geographic distances. Proc Natl Acad Sci USA 2019; 116:20568–20573 [View Article] [PubMed]
    [Google Scholar]
  11. Grohmann E, Christie PJ, Waksman G, Backert S. Type IV secretion in Gram-negative and Gram-positive bacteria. Mol Microbiol 2018; 107:455–471 [View Article] [PubMed]
    [Google Scholar]
  12. Petersen J, Wagner-Döbler I. Plasmid transfer in the ocean – a case study from the roseobacter group. Front Microbiol 2017; 8:1350 [View Article] [PubMed]
    [Google Scholar]
  13. Töpel M, Pinder MIM, Johansson ON, Kourtchenko O, Godhe A et al. Genome sequence of Roseovarius mucosus strain SMR3, isolated from a culture of the diatom Skeletonema marinoi. Genome Announc 2017; 5:e00394-17 [View Article] [PubMed]
    [Google Scholar]
  14. Patzelt D, Michael V, Päuker O, Ebert M, Tielen P et al. Gene flow across genus barriers – conjugation of Dinoroseobacter shibae’s 191-kb killer plasmid into Phaeobacter inhibens and AHL-mediated expression of type IV secretion systems. Front Microbiol 2016; 7:742 [View Article] [PubMed]
    [Google Scholar]
  15. Seyedsayamdost MR, Case RJ, Kolter R, Clardy J. The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis. Nat Chem 2011; 3:331–335 [View Article] [PubMed]
    [Google Scholar]
  16. Wang H, Tomasch J, Jarek M, Wagner-Döbler I. A dual-species co-cultivation system to study the interactions between roseobacters and dinoflagellates. Front Microbiol 2014; 5:311 [View Article] [PubMed]
    [Google Scholar]
  17. Segev E, Wyche TP, Kim KH, Petersen J, Ellebrandt C et al. Dynamic metabolic exchange governs a marine algal-bacterial interaction. elife 2016; 5:e17473 [View Article] [PubMed]
    [Google Scholar]
  18. Biebl H, Allgaier M, Tindall BJ, Koblizek M, Lünsdorf H et al. Dinoroseobacter shibae gen. nov., sp. nov., a new aerobic phototrophic bacterium isolated from dinoflagellates. Int J Syst Evol Microbiol 2005; 55:1089–1096 [View Article] [PubMed]
    [Google Scholar]
  19. Wagner-Döbler I, Ballhausen B, Berger M, Brinkhoff T, Buchholz I et al. The complete genome sequence of the algal symbiont Dinoroseobacter shibae: a hitchhiker’s guide to life in the sea. ISME J 2010; 4:61–77 [View Article] [PubMed]
    [Google Scholar]
  20. Wang H, Tomasch J, Michael V, Bhuju S, Jarek M et al. Identification of genetic modules mediating the Jekyll and Hyde interaction of Dinoroseobacter shibae with the Dinoflagellate Prorocentrum minimum. Front Microbiol 2015; 6:1262 [View Article] [PubMed]
    [Google Scholar]
  21. Martens T, Heidorn T, Pukall R, Simon M, Tindall BJ et al. Reclassification of Roseobacter gallaeciensis Ruiz-Ponte et al. 1998 as Phaeobacter gallaeciensis gen. nov., comb. nov., description of Phaeobacter inhibens sp. nov., reclassification of Ruegeria algicola (Lafay et al. 1995) Uchino et al. 1999 as Marinovum algicola gen. nov., comb. nov., and emended descriptions of the genera Roseobacter, Ruegeria and Leisingera. Int J Syst Evol Microbiol 2006; 56:1293–1304 [View Article] [PubMed]
    [Google Scholar]
  22. Ruiz-Ponte C, Cilia V, Lambert C, Nicolas JL. Roseobacter gallaeciensis sp. nov., a new marine bacterium isolated from rearings and collectors of the scallop Pecten maximus. Int J Syst Bacteriol 1998; 48:537–542 [View Article] [PubMed]
    [Google Scholar]
  23. Thole S, Kalhoefer D, Voget S, Berger M, Engelhardt T et al. Phaeobacter gallaeciensis genomes from globally opposite locations reveal high similarity of adaptation to surface life. ISME J 2012; 6:2229–2244 [View Article] [PubMed]
    [Google Scholar]
  24. Frank O, Michael V, Päuker O, Boedeker C, Jogler C et al. Plasmid curing and the loss of grip – the 65-kb replicon of Phaeobacter inhibens DSM 17395 is required for biofilm formation, motility and the colonization of marine algae. Syst Appl Microbiol 2015; 38:120–127 [View Article] [PubMed]
    [Google Scholar]
  25. Brock NL, Nikolay A, Dickschat JS. Biosynthesis of the antibiotic tropodithietic acid by the marine bacterium Phaeobacter inhibens. Chem Commun 2014; 50:5487–5489 [View Article] [PubMed]
    [Google Scholar]
  26. Berger M, Neumann A, Schulz S, Simon M, Brinkhoff T. Tropodithietic acid production in Phaeobacter gallaeciensis is regulated by N-acyl homoserine lactone-mediated quorum sensing. J Bacteriol 2011; 193:6576–6585 [View Article] [PubMed]
    [Google Scholar]
  27. Wilson MZ, Wang R, Gitai Z, Seyedsayamdost MR. Mode of action and resistance studies unveil new roles for tropodithietic acid as an anticancer agent and the γ-glutamyl cycle as a proton sink. Proc Natl Acad Sci USA 2016; 113:1630–1635 [View Article] [PubMed]
    [Google Scholar]
  28. Trautwein K, Will SE, Hulsch R, Maschmann U, Wiegmann K et al. Native plasmids restrict growth of Phaeobacter inhibens DSM 17395: energetic costs of plasmids assessed by quantitative physiological analyses. Environ Microbiol 2016; 18:4817–4829 [View Article] [PubMed]
    [Google Scholar]
  29. Will SE, Neumann-Schaal M, Heydorn RL, Bartling P, Petersen J et al. The limits to growth – energetic burden of the endogenous antibiotic tropodithietic acid in Phaeobacter inhibens DSM 17395. PLoS One 2017; 12:e0177295 [View Article] [PubMed]
    [Google Scholar]
  30. Bartling P, Vollmers J, Petersen J. The first world swimming championships of roseobacters – phylogenomic insights into an exceptional motility phenotype. Syst Appl Microbiol 2018; 41:544–554 [View Article] [PubMed]
    [Google Scholar]
  31. Stamatakis A. Using RAxML to infer phylogenies. Curr Protoc Bioinformatics 2015; 51:6.14.1–6.14.14 [View Article] [PubMed]
    [Google Scholar]
  32. Ebert M, Laaß S, Burghartz M, Petersen J, Koßmehl S et al. Transposon mutagenesis identified chromosomal and plasmid genes essential for adaptation of the marine bacterium Dinoroseobacter shibae to anaerobic conditions. J Bacteriol 2013; 195:4769–4777 [View Article] [PubMed]
    [Google Scholar]
  33. Bartling P, Brinkmann H, Bunk B, Overmann J, Göker M et al. The composite 259-kb plasmid of Martelella mediterranea DSM 17316t – a natural replicon with functional RepABC modules from Rhodobacteraceae and Rhizobiaceae. Front Microbiol 2017; 8:1787 [PubMed]
    [Google Scholar]
  34. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article] [PubMed]
    [Google Scholar]
  35. Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V et al. Twelve years of SAMtools and BCFtools. GigaScience 2021; 10:giab008 [View Article] [PubMed]
    [Google Scholar]
  36. Koboldt DC, Zhang Q, Larson DE, Shen D, McLellan MD et al. VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res 2012; 22:568–576 [View Article] [PubMed]
    [Google Scholar]
  37. Wickham H. Polishing your plots for publication. In ggplot2 vol 55 New York: Springer New York; 2009 pp 139–155
    [Google Scholar]
  38. Marie D, Partensky F, Jacquet S, Vaulot D. Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR green I. Appl Environ Microbiol 1997; 63:186–193 [View Article] [PubMed]
    [Google Scholar]
  39. Segev E, Tellez A, Vlamakis H, Kolter R. Morphological heterogeneity and attachment of Phaeobacter inhibens. PLoS One 2015; 10:e0141300 [View Article] [PubMed]
    [Google Scholar]
  40. Frank O, Pradella S, Rohde M, Scheuner C, Klenk H-P et al. Complete genome sequence of the Phaeobacter gallaeciensis type strain CIP 105210(T) (= DSM 26640(T) = BS107(T)). Stand Genomic Sci 2015; 9:914–932 [View Article] [PubMed]
    [Google Scholar]
  41. Cui L, Neoh H, Iwamoto A, Hiramatsu K. Coordinated phenotype switching with large-scale chromosome flip-flop inversion observed in bacteria. Proc Natl Acad Sci USA 2012; 109:E1647–E1656 [View Article] [PubMed]
    [Google Scholar]
  42. Birmes L, Freese HM, Petersen J. RepC_soli: a novel promiscuous plasmid type of Rhodobacteraceae mediates horizontal transfer of antibiotic resistances in the ocean. Environ Microbiol 2021; 23:5395–5411 [View Article] [PubMed]
    [Google Scholar]
  43. Kleist S, Ulbrich M, Bill N, Schmidt-Hohagen K, Geffers R et al. Dealing with salinity extremes and nitrogen limitation – an unexpected strategy of the marine bacterium Dinoroseobacter shibae. Environ Microbiol 2017; 19:894–908 [View Article] [PubMed]
    [Google Scholar]
  44. San Millan A, Toll-Riera M, Qi Q, Betts A, Hopkinson RJ et al. Integrative analysis of fitness and metabolic effects of plasmids in Pseudomonas aeruginosa PAO1. ISME J 2018; 12:3014–3024 [View Article] [PubMed]
    [Google Scholar]
  45. Mansky J, Wang H, Ebert M, Härtig E, Jahn D et al. The Influence of Genes on the “Killer Plasmid” of Dinoroseobacter shibae on Its Symbiosis With the Dinoflagellate Prorocentrum minimum. Front Microbiol 2022; 12: [View Article]
    [Google Scholar]
  46. Chen J, Quiles-Puchalt N, Chiang YN, Bacigalupe R, Fillol-Salom A et al. Genome hypermobility by lateral transduction. Science 2018; 362:207–212 [View Article] [PubMed]
    [Google Scholar]
  47. Tomasch J, Wang H, Hall ATK, Patzelt D, Preusse M et al. Packaging of Dinoroseobacter shibae DNA into gene transfer agent particles is not random. Genome Biol Evol 2018; 10:359–369 [View Article] [PubMed]
    [Google Scholar]
  48. Buchan A, González JM, Moran MA. Overview of the marine roseobacter lineage. Appl Environ Microbiol 2005; 71:5665–5677 [View Article] [PubMed]
    [Google Scholar]
  49. Fiebig A, Pradella S, Petersen J, Michael V, Päuker O et al. Genome of the marine alphaproteobacterium Hoeflea phototrophica type strain (DFL-43T). Stand Genomic Sci 2013; 7:440–448 [View Article] [PubMed]
    [Google Scholar]
  50. Liu Y, Zheng Q, Lin W, Jiao N. Characteristics and evolutionary analysis of photosynthetic gene clusters on extrachromosomal replicons: from streamlined plasmids to chromids. mSystems 2019; 4:e00358-19 [View Article] [PubMed]
    [Google Scholar]
  51. Petersen J, Brinkmann H, Bunk B, Michael V, Päuker O et al. Think pink: photosynthesis, plasmids and the Roseobacter clade. Environ Microbiol 2012; 14:2661–2672 [View Article] [PubMed]
    [Google Scholar]
  52. Brinkmann H, Göker M, Koblížek M, Wagner-Döbler I, Petersen J. Horizontal operon transfer, plasmids, and the evolution of photosynthesis in Rhodobacteraceae. ISME J 2018; 12:1994–2010 [View Article] [PubMed]
    [Google Scholar]
  53. Seymour JR, Amin SA, Raina JB, Stocker R. Zooming in on the phycosphere: the ecological interface for phytoplankton-bacteria relationships. Nat Microbiol 2017; 2:17065 [View Article] [PubMed]
    [Google Scholar]
  54. Pinto UM, Pappas KM, Winans SC. The ABCs of plasmid replication and segregation. Nat Rev Microbiol 2012; 10:755–765 [View Article] [PubMed]
    [Google Scholar]
  55. Caplan A, Herrera-Estrella L, Inzé D, Van Haute E, Van Montagu M et al. Introduction of genetic material into plant cells. Science 1983; 222:815–821 [View Article] [PubMed]
    [Google Scholar]
  56. Gordon JE, Christie PJ. The Agrobacterium Ti plasmids. Microbiol Spectr 2014; 2:2.6.19 [View Article] [PubMed]
    [Google Scholar]
  57. Vaghchhipawala Z, Radke S, Nagy E, Russell ML, Johnson S et al. RepB C-terminus mutation of a pRi-repABC binary vector affects plasmid copy number in Agrobacterium and transgene copy number in plants. PLoS One 2018; 13:e0200972 [View Article] [PubMed]
    [Google Scholar]
  58. Fournes F, Val ME, Skovgaard O, Mazel D. Replicate once per cell cycle: replication control of secondary chromosomes. Front Microbiol 2018; 9:01833 [View Article] [PubMed]
    [Google Scholar]
  59. López JL, Lozano MJ, Lagares A, Fabre ML, Draghi WO et al. Codon usage heterogeneity in the multipartite prokaryote genome: selection-based coding bias associated with gene location, expression level, and ancestry. mBio 2019; 10:e00505-19 [View Article] [PubMed]
    [Google Scholar]
  60. Petersen J, Brinkmann H, Pradella S. Diversity and evolution of repABC type plasmids in Rhodobacterales. Environ Microbiol 2009; 11:2627–2638 [View Article] [PubMed]
    [Google Scholar]
  61. Yamaguchi Y, Park JH, Inouye M. Toxin-antitoxin systems in bacteria and archaea. Annu Rev Genet 2011; 45:61–79 [View Article] [PubMed]
    [Google Scholar]
  62. Bramucci AR, Labeeuw L, Orata FD, Ryan EM, Malmstrom RR et al. The bacterial symbiont Phaeobacter inhibens shapes the life history of its algal host Emiliania huxleyi. Front Mar Sci 2018; 5:188
    [Google Scholar]
  63. Bramucci AR, Case RJ. Phaeobacter inhibens induces apoptosis-like programmed cell death in calcifying Emiliania huxleyi. Sci Rep 2019; 9:5215 [View Article] [PubMed]
    [Google Scholar]
  64. Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG. Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 2005; 438:90–93 [View Article] [PubMed]
    [Google Scholar]
  65. Croft MT, Warren MJ, Smith AG. Algae need their vitamins. Eukaryot Cell 2006; 5:1175–1183 [View Article] [PubMed]
    [Google Scholar]
  66. Wienhausen G, Noriega-Ortega BE, Niggemann J, Dittmar T, Simon M. The exometabolome of two model strains of the Roseobacter group: a marketplace of microbial metabolites. Front Microbiol 2017; 8:1985 [View Article] [PubMed]
    [Google Scholar]
  67. Cooper MB, Kazamia E, Helliwell KE, Kudahl UJ, Sayer A et al. Cross-exchange of B-vitamins underpins a mutualistic interaction between Ostreococcus tauri and Dinoroseobacter shibae. ISME J 2019; 13:334–345 [View Article] [PubMed]
    [Google Scholar]
  68. Amin SA, Hmelo LR, van Tol HM, Durham BP, Carlson LT et al. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 2015; 522:98–101 [View Article] [PubMed]
    [Google Scholar]
  69. Wichard T. Exploring bacteria-induced growth and morphogenesis in the green macroalga order Ulvales (Chlorophyta). Front Plant Sci 2015; 6:86 [View Article] [PubMed]
    [Google Scholar]
  70. Christie-Oleza JA, Sousoni D, Lloyd M, Armengaud J, Scanlan DJ. Nutrient recycling facilitates long-term stability of marine microbial phototroph-heterotroph interactions. Nat Microbiol 2017; 2:17100 [View Article] [PubMed]
    [Google Scholar]
  71. Teyssier-Cuvelle S, Mougel C, Nesme X. Direct conjugal transfers of Ti plasmid to soil microflora. Mol Ecol 1999; 8:1273–1284 [View Article] [PubMed]
    [Google Scholar]
  72. Pilla G, Tang CM. Going around in circles: virulence plasmids in enteric pathogens. Nat Rev Microbiol 2018; 16:484–495 [View Article] [PubMed]
    [Google Scholar]
  73. Schuenemann VJ, Bos K, DeWitte S, Schmedes S, Jamieson J et al. Targeted enrichment of ancient pathogens yielding the pPCP1 plasmid of Yersinia pestis from victims of the Black Death. Proc Natl Acad Sci USA 2011; 108:E746–E752 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000787
Loading
/content/journal/mgen/10.1099/mgen.0.000787
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL
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