Academic Journal
Mobile genetic elements shape the evolution and adaptation of the marine Sulfitobacter genus.
| Title: | Mobile genetic elements shape the evolution and adaptation of the marine Sulfitobacter genus. |
|---|---|
| Authors: | Guzel M; Department of Microbiology, University of Tennessee, Knoxville, Tennessee, USA.; Department of Food Engineering, Hitit University, Corum, Türkiye., May F; Department of Microbiology, University of Tennessee, Knoxville, Tennessee, USA., Buchan A; Department of Microbiology, University of Tennessee, Knoxville, Tennessee, USA. |
| Source: | MSystems [mSystems] 2026 Jul 21; Vol. 11 (7), pp. e0047926. Date of Electronic Publication: 2026 Jun 15. |
| Publication Type: | Journal Article |
| Language: | English |
| Journal Info: | Publisher: American Society for Microbiology Country of Publication: United States NLM ID: 101680636 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 2379-5077 (Electronic) Linking ISSN: 23795077 NLM ISO Abbreviation: mSystems Subsets: MEDLINE |
| Imprint Name(s): | Original Publication: Washington, DC : American Society for Microbiology, [2016]- |
| MeSH Terms: | Rhodobacteraceae*/genetics , Rhodobacteraceae*/classification , Rhodobacteraceae*/physiology , Adaptation, Physiological*/genetics , Evolution, Molecular* , Interspersed Repetitive Sequences*, Plasmids/genetics ; Chromosomes, Bacterial/genetics ; Gene Transfer, Horizontal ; Genome, Bacterial ; Phylogeny |
| Abstract: | Mobile genetic elements (MGEs) are essential for facilitating horizontal gene transfer and play crucial roles in the evolution and adaptive capabilities of bacterial species. Here, we analyzed closed genomes from the marine Sulfitobacter genus to assess plasmid contributions to ecological adaptability and evolutionary diversification. Our analysis of 153 Sulfitobacter plasmids from 36 strains representing 8 species shows extensive plasmid conservation within species (e.g., >95% nucleotide identity for flagellar plasmids) alongside significant mosaicism across 60% of plasmids. Insertion sequences (IS) elements are nearly ninefold more concentrated on plasmids relative to chromosomes, suggestive of active genetic exchange in this replicon class. Network analysis identified 14 primary plasmid clusters, with species-specific conservation patterns and evidence of inter-species gene transfer. In Sulfitobacter pontiacus strain CB2047, we discovered chromosomal integration of a 280 kb plasmid encoding a toxin-antitoxin system, rrn operon, as well as a chromosomal partitioning system. These findings demonstrate that plasmids function as key drivers of evolution and adaptation in Sulfitobacter, serving as both repositories of conserved adaptive traits and platforms for ongoing genetic innovation. Importance: Plasmids are increasingly recognized as crucial drivers of bacterial evolution and adaptation, yet their roles in shaping marine microbial communities are poorly understood. Here, we provide a comprehensive analysis of plasmid diversity and evolution within Sulfitobacter, a broadly distributed and metabolically versatile marine bacterial genus, in which ~15% of genome content is plasmid-encoded. We propose that Sulfitobacter plasmids serve dual evolutionary roles: maintaining highly conserved species-specific traits essential for survival (such as flagellar motility and biofilm formation), while simultaneously functioning as platforms for genetic innovation through extensive horizontal gene transfer. The discovery of a large plasmid integrated into the chromosome of one strain highlights that episomal elements can transition to stable chromosomal inheritance in this genus. These findings advance our understanding of how marine bacteria balance genomic stability with adaptive flexibility, providing insights applicable to microbial evolution in dynamic ocean environments. |
| Competing Interests: | The authors declare no conflict of interest. |
| References: | Bioinformatics. 2015 Oct 15;31(20):3350-2. (PMID: 26099265) Genome Biol. 2003;4(1):203. (PMID: 12540296) Crit Rev Microbiol. 2017 Nov;43(6):709-730. (PMID: 28407717) mBio. 2023 Jun 27;14(3):e0315822. (PMID: 37097157) Bioinformatics. 2015 Nov 15;31(22):3691-3. (PMID: 26198102) PLoS One. 2010 Jun 25;5(6):e11147. (PMID: 20593022) Bioinformatics. 2018 Sep 1;34(17):i884-i890. (PMID: 30423086) Mol Biol Evol. 2022 Jun 2;39(6):. (PMID: 35639760) Nat Rev Microbiol. 2012 Nov;10(11):755-65. (PMID: 23070556) Nat Rev Microbiol. 2005 Sep;3(9):722-32. (PMID: 16138100) mSystems. 2022 Aug 30;7(4):e0026422. (PMID: 35920548) PeerJ. 2015 Oct 08;3:e1319. (PMID: 26500826) Microb Genom. 2024 Oct;10(10):. (PMID: 39401066) ISME J. 2017 Jun;11(6):1483-1499. (PMID: 28106881) Mol Biol Evol. 2013 Apr;30(4):772-80. (PMID: 23329690) Bioinformatics. 2014 May 1;30(9):1312-3. (PMID: 24451623) Microb Genom. 2022 Mar;8(3):. (PMID: 35254236) Microbiology (Reading). 2022 Jul;168(7):. (PMID: 35849537) Genome Biol Evol. 2017 Dec 1;9(12):3297-3311. (PMID: 29194520) Toxins (Basel). 2021 Jul 08;13(7):. (PMID: 34357945) Proc Natl Acad Sci U S A. 2019 Oct 8;116(41):20568-20573. (PMID: 31548387) Plasmid. 2019 Mar;102:10-18. (PMID: 30797764) Nucleic Acids Res. 2014 Nov 10;42(20):12333-51. (PMID: 25324310) Nat Ecol Evol. 2021 Dec;5(12):1624-1636. (PMID: 34750532) mSphere. 2022 Apr 27;7(2):e0093021. (PMID: 35311569) Appl Microbiol Biotechnol. 2013 Apr;97(7):2805-15. (PMID: 23435940) PLoS Comput Biol. 2017 Jun 8;13(6):e1005595. (PMID: 28594827) BMC Genomics. 2024 Apr 22;25(1):389. (PMID: 38649849) CRISPR J. 2020 Dec;3(6):462-469. (PMID: 33275853) Nucleic Acids Res. 2022 Jul 5;50(W1):W541-W550. (PMID: 35639517) Bioinformatics. 2017 Nov 01;33(21):3340-3347. (PMID: 29077810) Microbiol Spectr. 2022 Feb 23;10(1):e0222521. (PMID: 34985328) Front Microbiol. 2016 May 31;7:742. (PMID: 27303368) Nucleic Acids Res. 2018 Jul 2;46(W1):W200-W204. (PMID: 29905871) Front Microbiol. 2021 Jun 25;12:683109. (PMID: 34248901) Mol Microbiol. 2009 Nov;74(3):557-81. (PMID: 19737356) Environ Microbiol. 2015 Oct;17(10):4019-34. (PMID: 26079637) Microorganisms. 2022 Mar 29;10(4):. (PMID: 35456790) Microb Genom. 2018 Aug;4(8):. (PMID: 30052170) Microbiol Mol Biol Rev. 2010 Sep;74(3):434-52. (PMID: 20805406) Annu Rev Microbiol. 2006;60:255-80. (PMID: 16719716) Nat Rev Microbiol. 2021 Jul;19(7):442-453. (PMID: 33846600) Res Microbiol. 2004 Jun;155(5):387-98. (PMID: 15207871) ISME J. 2020 Jul;14(7):1688-1700. (PMID: 32242083) Microbiol Spectr. 2015 Apr;3(2):MDNA3-0030-2014. (PMID: 26104715) Nat Biotechnol. 2024 Aug;42(8):1303-1312. (PMID: 37735266) Proc Natl Acad Sci U S A. 2009 Nov 10;106(45):19126-31. (PMID: 19855009) Microbiol Mol Biol Rev. 2014 Dec;78(4):573-87. (PMID: 25428935) Microbiol Mol Biol Rev. 1998 Sep;62(3):725-74. (PMID: 9729608) ISME J. 2018 Aug;12(8):1994-2010. (PMID: 29795276) J Mol Biol. 1976 Nov 5;107(3):207-22. (PMID: 794483) ISME J. 2016 Oct;10(10):2498-513. (PMID: 26953602) Nucleic Acids Res. 2021 Sep 20;49(16):9077-9096. (PMID: 34417604) Mol Biol Evol. 2007 Apr;24(4):969-81. (PMID: 17251179) Bioinformatics. 2018 Sep 15;34(18):3094-3100. (PMID: 29750242) Mol Biol Evol. 2011 Mar;28(3):1229-40. (PMID: 21097494) Appl Environ Microbiol. 2005 Oct;71(10):5665-77. (PMID: 16204474) Bioinformatics. 2014 Jul 15;30(14):2068-9. (PMID: 24642063) Mob DNA. 2019 Oct 9;10:40. (PMID: 31624505) |
| Grant Information: | OCE-1737237 National Science Foundation; 735083 Simons Foundation |
| Contributed Indexing: | Keywords: Roseobacteraceae; Sulfitobacter; horizontal gene transfer; mobile genetic element; plasmid |
| Entry Date(s): | Date Created: 20260615 Date Completed: 20260721 Latest Revision: 20260813 |
| Update Code: | 20260813 |
| PubMed Central ID: | PMC13386836 |
| DOI: | 10.1128/msystems.00479-26 |
| PMID: | 42294647 |
| Database: | MEDLINE |
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| Items | – Name: Title Label: Title Group: Ti Data: Mobile genetic elements shape the evolution and adaptation of the marine Sulfitobacter genus. – Name: Author Label: Authors Group: Au Data: <searchLink fieldCode="AU" term="%22Guzel+M%22">Guzel M</searchLink>; Department of Microbiology, University of Tennessee, Knoxville, Tennessee, USA.; Department of Food Engineering, Hitit University, Corum, Türkiye.<br /><searchLink fieldCode="AU" term="%22May+F%22">May F</searchLink>; Department of Microbiology, University of Tennessee, Knoxville, Tennessee, USA.<br /><searchLink fieldCode="AU" term="%22Buchan+A%22">Buchan A</searchLink>; Department of Microbiology, University of Tennessee, Knoxville, Tennessee, USA. – Name: TitleSource Label: Source Group: Src Data: <searchLink fieldCode="JN" term="%22101680636%22">MSystems</searchLink> [mSystems] 2026 Jul 21; Vol. 11 (7), pp. e0047926. <i>Date of Electronic Publication: </i>2026 Jun 15. – Name: TypePub Label: Publication Type Group: TypPub Data: Journal Article – Name: Language Label: Language Group: Lang Data: English – Name: TitleSource Label: Journal Info Group: Src Data: <i>Publisher: </i><searchLink fieldCode="PB" term="%22American+Society+for+Microbiology%22">American Society for Microbiology </searchLink><i>Country of Publication: </i>United States <i>NLM ID: </i>101680636 <i>Publication Model: </i>Print-Electronic <i>Cited Medium: </i>Internet <i>ISSN: </i>2379-5077 (Electronic) <i>Linking ISSN: </i><searchLink fieldCode="IS" term="%2223795077%22">23795077 </searchLink><i>NLM ISO Abbreviation: </i>mSystems <i>Subsets: </i>MEDLINE – Name: PublisherInfo Label: Imprint Name(s) Group: PubInfo Data: <i>Original Publication</i>: Washington, DC : American Society for Microbiology, [2016]- – Name: SubjectMESH Label: MeSH Terms Group: Su Data: <searchLink fieldCode="MM" term="%22Rhodobacteraceae%22">Rhodobacteraceae*</searchLink>/<searchLink fieldCode="MM" term="%22Rhodobacteraceae+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Rhodobacteraceae%22">Rhodobacteraceae*</searchLink>/<searchLink fieldCode="MM" term="%22Rhodobacteraceae+classification%22">classification</searchLink> <br /><searchLink fieldCode="MM" term="%22Rhodobacteraceae%22">Rhodobacteraceae*</searchLink>/<searchLink fieldCode="MM" term="%22Rhodobacteraceae+physiology%22">physiology</searchLink> <br /><searchLink fieldCode="MM" term="%22Adaptation%2C+Physiological%22">Adaptation, Physiological*</searchLink>/<searchLink fieldCode="MM" term="%22Adaptation%2C+Physiological+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Evolution%2C+Molecular%22">Evolution, Molecular*</searchLink> <br /><searchLink fieldCode="MM" term="%22Interspersed+Repetitive+Sequences%22">Interspersed Repetitive Sequences*</searchLink><br /><searchLink fieldCode="MH" term="%22Plasmids%22">Plasmids</searchLink>/<searchLink fieldCode="MH" term="%22Plasmids+genetics%22">genetics</searchLink> ; <searchLink fieldCode="MH" term="%22Chromosomes%2C+Bacterial%22">Chromosomes, Bacterial</searchLink>/<searchLink fieldCode="MH" term="%22Chromosomes%2C+Bacterial+genetics%22">genetics</searchLink> ; <searchLink fieldCode="MH" term="%22Gene+Transfer%2C+Horizontal%22">Gene Transfer, Horizontal</searchLink> ; <searchLink fieldCode="MH" term="%22Genome%2C+Bacterial%22">Genome, Bacterial</searchLink> ; <searchLink fieldCode="MH" term="%22Phylogeny%22">Phylogeny</searchLink> – Name: Abstract Label: Abstract Group: Ab Data: Mobile genetic elements (MGEs) are essential for facilitating horizontal gene transfer and play crucial roles in the evolution and adaptive capabilities of bacterial species. Here, we analyzed closed genomes from the marine Sulfitobacter genus to assess plasmid contributions to ecological adaptability and evolutionary diversification. Our analysis of 153 Sulfitobacter plasmids from 36 strains representing 8 species shows extensive plasmid conservation within species (e.g., >95% nucleotide identity for flagellar plasmids) alongside significant mosaicism across 60% of plasmids. Insertion sequences (IS) elements are nearly ninefold more concentrated on plasmids relative to chromosomes, suggestive of active genetic exchange in this replicon class. Network analysis identified 14 primary plasmid clusters, with species-specific conservation patterns and evidence of inter-species gene transfer. In Sulfitobacter pontiacus strain CB2047, we discovered chromosomal integration of a 280 kb plasmid encoding a toxin-antitoxin system, rrn operon, as well as a chromosomal partitioning system. These findings demonstrate that plasmids function as key drivers of evolution and adaptation in Sulfitobacter, serving as both repositories of conserved adaptive traits and platforms for ongoing genetic innovation.<br />Importance: Plasmids are increasingly recognized as crucial drivers of bacterial evolution and adaptation, yet their roles in shaping marine microbial communities are poorly understood. Here, we provide a comprehensive analysis of plasmid diversity and evolution within Sulfitobacter, a broadly distributed and metabolically versatile marine bacterial genus, in which ~15% of genome content is plasmid-encoded. We propose that Sulfitobacter plasmids serve dual evolutionary roles: maintaining highly conserved species-specific traits essential for survival (such as flagellar motility and biofilm formation), while simultaneously functioning as platforms for genetic innovation through extensive horizontal gene transfer. The discovery of a large plasmid integrated into the chromosome of one strain highlights that episomal elements can transition to stable chromosomal inheritance in this genus. These findings advance our understanding of how marine bacteria balance genomic stability with adaptive flexibility, providing insights applicable to microbial evolution in dynamic ocean environments. – Name: Abstract Label: Competing Interests Group: Ab Data: The authors declare no conflict of interest. – Name: Ref Label: References Group: RefInfo Data: Bioinformatics. 2015 Oct 15;31(20):3350-2. (PMID: <searchLink fieldCode="PM" term="%2226099265%22">26099265)</searchLink><br />Genome Biol. 2003;4(1):203. (PMID: <searchLink fieldCode="PM" term="%2212540296%22">12540296)</searchLink><br />Crit Rev Microbiol. 2017 Nov;43(6):709-730. (PMID: <searchLink fieldCode="PM" term="%2228407717%22">28407717)</searchLink><br />mBio. 2023 Jun 27;14(3):e0315822. 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(PMID: <searchLink fieldCode="PM" term="%2231624505%22">31624505)</searchLink> – Name: GrantInfo Label: Grant Information Group: Grant Data: OCE-1737237 National Science Foundation; 735083 Simons Foundation – Name: SubjectMinor Label: Contributed Indexing Group: Data: <i>Keywords: </i>Roseobacteraceae; Sulfitobacter; horizontal gene transfer; mobile genetic element; plasmid – Name: DateEntry Label: Entry Date(s) Group: Date Data: <i>Date Created: </i>20260615 <i>Date Completed: </i>20260721 <i>Latest Revision: </i>20260813 – Name: DateUpdate Label: Update Code Group: Date Data: 20260813 – Name: PubmedCentralID Label: PubMed Central ID Group: ID Data: PMC13386836 – Name: DOI Label: DOI Group: ID Data: 10.1128/msystems.00479-26 – Name: AN Label: PMID Group: ID Data: 42294647 |
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| RecordInfo | BibRecord: BibEntity: Identifiers: – Type: doi Value: 10.1128/msystems.00479-26 Languages: – Code: eng Text: English PhysicalDescription: Pagination: StartPage: e0047926 Subjects: – SubjectFull: Plasmids genetics Type: general – SubjectFull: Chromosomes, Bacterial genetics Type: general – SubjectFull: Gene Transfer, Horizontal Type: general – SubjectFull: Genome, Bacterial Type: general – SubjectFull: Phylogeny Type: general – SubjectFull: Rhodobacteraceae genetics Type: general – SubjectFull: Rhodobacteraceae classification Type: general – SubjectFull: Rhodobacteraceae physiology Type: general – SubjectFull: Adaptation, Physiological genetics Type: general – SubjectFull: Evolution, Molecular Type: general – SubjectFull: Interspersed Repetitive Sequences Type: general Titles: – TitleFull: Mobile genetic elements shape the evolution and adaptation of the marine Sulfitobacter genus. Type: main BibRelationships: HasContributorRelationships: – PersonEntity: Name: NameFull: Guzel M – PersonEntity: Name: NameFull: May F – PersonEntity: Name: NameFull: Buchan A IsPartOfRelationships: – BibEntity: Dates: – D: 21 M: 07 Text: 2026 Jul 21 Type: published Y: 2026 Identifiers: – Type: issn-electronic Value: 2379-5077 Numbering: – Type: volume Value: 11 – Type: issue Value: 7 Titles: – TitleFull: MSystems Type: main |
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