• This record comes from PubMed

Structural and regulatory determinants of flagellar motility in Rhodobacterales - The archetypal flagellum of Phaeobacter inhibens DSM 17395

. 2025 Mar 24 ; () : . [epub] 20250324

Status PubMed-not-MEDLINE Language English Country United States Media electronic

Document type Journal Article, Preprint

Flagellar motility is crucial for the swim-and-stick lifestyle of Rhodobacterales and plays an important role for bacterial-algal interactions. This alphaproteobacterial order contains three distinct types of flagellar gene clusters (FGCs) for the formation of a functional flagellum. Our phylogenetically broad taxon sampling of more than 300 genomes revealed that the most common FGC, the fla1-type, was probably already present in the common ancestor of Rhodobacterales and was strictly vertically inherited, while the other two FGC types, fla2 and fla3, were spread via horizontal operon transfers. Swimming of the marine model organism Phaeobacter inhibens DSM 17395 (Roseobacteraceae) is mediated by the archetypal fla1-type flagellum. Screening of 13,000 transposon mutants of P. inhibens on soft agar plates revealed that 40 genes, including four genes encoding conserved but not yet characterized proteins (CP1-4) within the FGC, are essential for motility. Exoproteome analyses indicated that CP1-4 are required at different stages of flagellar assembly. Only eight genes outside the FGC were identified as essential for swimming motility, including all three genes of the CtrA phosphorelay. Using comparative transcriptomics of ΔcckA, ΔchpT and ΔctrA mutants of the distantly related model organisms P. inhibens and Dinoroseobacter shibae DFL 12, we identified genes for the flagellum and cyclic di-GMP turnover as core targets of the CtrA phosphorelay and a conserved connection with quorum sensing across members of the Rhodobacterales.

Update In

PubMed

See more in PubMed

Liang KYH, Orata FD, Boucher YF, Case RJ. Roseobacters in a Sea of Poly- and Paraphyly: Whole Genome-Based Taxonomy of the Family Rhodobacteraceae and the Proposal for the Split of the “Roseobacter Clade” Into a Novel Family, Roseobacteraceae fam. nov. Front Microbiol. 2021;12. doi: 10.3389/fmicb.2021.683109 PubMed DOI PMC

Huang Z, Li M, Oren A, Lai Q. Genome-based analysis of the family Paracoccaceae and description of Ostreiculturibacter nitratireducens gen. nov., sp. nov., isolated from an oyster farm on a tidal flat. Front Microbiol. 2024;15. doi: 10.3389/fmicb.2024.1376777 PubMed DOI PMC

Simon M, Scheuner C, Meier-Kolthoff JP, Brinkhoff T, Wagner-Döbler I, Ulbrich M, et al. Phylogenomics of Rhodobacteraceae reveals evolutionary adaptation to marine and non-marine habitats. ISME J. 2017;11: 1483–1499. doi: 10.1038/ismej.2016.198 PubMed DOI PMC

Wichard T. Exploring bacteria-induced growth and morphogenesis in the green macroalga order Ulvales (Chlorophyta). Front Plant Sci. 2015;6. doi: 10.3389/fpls.2015.00086 PubMed DOI PMC

Segev E, Wyche TP, Kim KH, Petersen J, Ellebrandt C, Vlamakis H, et al. Dynamic metabolic exchange governs a marine algal-bacterial interaction. Falkowski PG, editor. eLife. 2016;5: e17473. doi: 10.7554/eLife.17473 PubMed DOI PMC

Fei C, Ochsenkühn MA, Shibl AA, Isaac A, Wang C, Amin SA. Quorum sensing regulates ‘swim-or-stick’ lifestyle in the phycosphere. Environmental Microbiology. 2020;22: 4761–4778. doi: 10.1111/1462-2920.15228 PubMed DOI PMC

Isaac A, Mohamed AR, Amin SA. Rhodobacteraceae are key players in microbiome assembly of the diatom Asterionellopsis glacialis. Applied and Environmental Microbiology. 2024;90: e00570–24. doi: 10.1128/aem.00570-24 PubMed DOI PMC

Fei C, Booker A, Klass S, Vidyarathna NK, Ahn SH, Mohamed AR, et al. Friends and foes: symbiotic and algicidal bacterial influence on Karenia brevis blooms. ISME Communications. 2025;5: ycae164. doi: 10.1093/ismeco/ycae164 PubMed DOI PMC

Qui-Minet ZN, Wichard T, Del Olmo G, Pereira M, Holbl H, Ruiz P, et al. Light-regulated interactions between Phaeobacter sp. and Ulva ohnoi (Chlorophyta): Effects on microbiome dynamics, metabolome composition, and tropodithietic acid production. Environmental and Experimental Botany. 2025;230: 106093. doi: 10.1016/j.envexpbot.2025.106093 DOI

Wagner-Döbler I, Biebl H. Environmental Biology of the Marine Roseobacter Lineage. Annual Review of Microbiology. 2006;60: 255–280. doi: 10.1146/annurev.micro.60.080805.142115 PubMed DOI

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. doi: 10.1038/nrmicro3326 PubMed DOI

Wienhausen G, Moraru C, Bruns S, Tran DQ, Sultana S, Wilkes H, et al. Ligand cross-feeding resolves bacterial vitamin B12 auxotrophies. Nature. 2024;629: 886–892. doi: 10.1038/s41586-024-07396-y PubMed DOI

Wang H, Tomasch J, Jarek M, Wagner-Döbler I. A dual-species co-cultivation system to study the interactions between Roseobacters and dinoflagellates. Frontiers in microbiology. 2014;5: 311. doi: 10.3389/fmicb.2014.00311 PubMed DOI PMC

Tomasch J, Ringel V, Wang H, Freese HM, Bartling P, Brinkmann H, et al. Fatal affairs–conjugational transfer of a dinoflagellate-killing plasmid between marine Rhodobacterales. Microbial genomics. 2022;8. doi: 10.1099/mgen.0.000787 PubMed DOI PMC

Abada A, Beiralas R, Narvaez D, Sperfeld M, Duchin-Rapp Y, Lipsman V, et al. Aerobic bacteria produce nitric oxide via denitrification and promote algal population collapse. The ISME Journal. 2023;17: 1167–1183. doi: 10.1038/s41396-023-01427-8 PubMed DOI PMC

Miller TR, Belas R. Motility is involved in Silicibacter sp. TM1040 interaction with dinoflagellates. Environmental Microbiology. 2006;8: 1648–1659. doi: 10.1111/j.1462-2920.2006.01071.x PubMed DOI

Frank O, Michael V, Päuker O, Boedeker C, Jogler C, Rohde M, et al. Plasmid curing and the loss of grip – The 65-kb replicon of PubMed DOI

Wang H, Tomasch J, Michael V, Bhuju S, Jarek M, Petersen J, et al. Identification of genetic modules mediating the Jekyll and Hyde interaction of Dinoroseobacter shibae with the dinoflagellate Prorocentrum minimum. Frontiers in Microbiology. 2015;6: 1262. doi: 10.3389/fmicb.2015.01262 PubMed DOI PMC

Michael V, Frank O, Bartling P, Scheuner C, Göker M, Brinkmann H, et al. Biofilm plasmids with a rhamnose operon are widely distributed determinants of the ‘swim-or-stick’ lifestyle in roseobacters. The ISME Journal. 2016;10: 2498–2513. doi: 10.1038/ismej.2016.30 PubMed DOI PMC

Bartling P, Vollmers J, Petersen J. The first world swimming championships of roseobacters—Phylogenomic insights into an exceptional motility phenotype. Systematic and Applied Microbiology. 2018;41: 544–554. doi: 10.1016/j.syapm.2018.08.012 PubMed DOI

Stocker R, Seymour JR. Ecology and Physics of Bacterial Chemotaxis in the Ocean . Microbiology and Molecular Biology Reviews. 2012;76: 792–812. doi: 10.1128/mmbr.00029-12 PubMed DOI PMC

Martínez-Pérez C, Zweifel ST, Pioli R, Stocker R. Space, the final frontier: The spatial component of phytoplankton–bacterial interactions. Molecular Microbiology. 2024;122: 331–346. doi: 10.1111/mmi.15293 PubMed DOI

Lasker K, Mann TH, Shapiro L. An intracellular compass spatially coordinates cell cycle modules in PubMed DOI PMC

Teeseling MCF van, Thanbichler M. Generating asymmetry in a changing environment: cell cycle regulation in dimorphic alphaproteobacteria. Biological Chemistry. 2020;401: 1349–1363. doi: 10.1515/hsz-2020-0235 PubMed DOI

Macnab RM. How Bacteria Assemble Flagella. Annual Review of Microbiology. 2003;57: 77–100. doi: 10.1146/annurev.micro.57.030502.090832 PubMed DOI

Chevance FFV, Hughes KT. Coordinating assembly of a bacterial macromolecular machine. Nat Rev Microbiol. 2008;6: 455–465. doi: 10.1038/nrmicro1887 PubMed DOI PMC

Wadhwa N, Berg HC. Bacterial motility: machinery and mechanisms. Nat Rev Microbiol. 2022;20: 161–173. doi: 10.1038/s41579-021-00626-4 PubMed DOI

Colin R, Ni B, Laganenka L, Sourjik V. Multiple functions of flagellar motility and chemotaxis in bacterial physiology. FEMS Microbiology Reviews. 2021;45: fuab038. doi: 10.1093/femsre/fuab038 PubMed DOI PMC

García N, Campos A, Osorio A, Poggio S, González-Pedrajo B, Camarena L, et al. The Flagellar Switch Genes fliM and fliN ofRhodobacter sphaeroides Are Contained in a Large Flagellar Gene Cluster. Journal of Bacteriology. 1998;180: 3978–3982. doi: 10.1128/jb.180.15.3978-3982.1998 PubMed DOI PMC

Frank O, Göker M, Pradella S, Petersen J. Ocean’s Twelve: flagellar and biofilm chromids in the multipartite genome of arinovum algicola DG898 exemplify functional compartmentalization. Environmental Microbiology. 2015;17: 4019–4034. doi: 10.1111/1462-2920.12947 PubMed DOI

Koppenhöfer S, Wang H, Scharfe M, Kaever V, Wagner-Döbler I, Tomasch J. Integrated Transcriptional Regulatory Network of Quorum Sensing, Replication Control, and SOS Response in Dinoroseobacter shibae. Frontiers in Microbiology. 2019;10. Available: https://www.frontiersin.org/articles/10.3389/fmicb.2019.00803 PubMed DOI PMC

Sonnenschein EC, Jimenez G, Castex M, Gram L. The Roseobacter-Group Bacterium Phaeobacter as a Safe Probiotic Solution for Aquaculture. Applied and Environmental Microbiology. 2021;87: e02581–20. doi: 10.1128/AEM.02581-20 PubMed DOI PMC

Drüppel K, Hensler M, Trautwein K, Koßmehl S, Wöhlbrand L, Schmidt-Hohagen K, et al. Pathways and substrate-specific regulation of amino acid degradation in haeobacter inhibens DSM 17395 (archetype of the marine oseobacter clade). Environmental Microbiology. 2014;16: 218–238. doi: 10.1111/1462-2920.12276 PubMed DOI

Trautwein K, Hensler M, Wiegmann K, Skorubskaya E, Wöhlbrand L, Wünsch D, et al. The marine bacterium Phaeobacter inhibens secures external ammonium by rapid buildup of intracellular nitrogen stocks. FEMS Microbiology Ecology. 2018;94: fiy154. doi: 10.1093/femsec/fiy154 PubMed DOI PMC

Petersen J, Brinkmann H, Berger M, Brinkhoff T, Päuker O, Pradella S. Origin and Evolution of a Novel DnaA-Like Plasmid Replication Type in Rhodobacterales. Molecular Biology and Evolution. 2011;28: 1229–1240. doi: 10.1093/molbev/msq310 PubMed DOI

Trautwein K, Will SE, Hulsch R, Maschmann U, Wiegmann K, Hensler M, et al. Native plasmids restrict growth of Phaeobacter inhibens DSM 17395: Energetic costs of plasmids assessed by quantitative physiological analyses. Environmental Microbiology. 2016;18: 4817–4829. doi: 10.1111/1462-2920.13381 PubMed DOI

Wünsch D, Strijkstra A, Wöhlbrand L, Freese HM, Scheve S, Hinrichs C, et al. Global Response of Phaeobacter inhibens DSM 17395 to Deletion of Its 262-kb Chromid Encoding Antibiotic Synthesis. Microbial Physiology. 2020;30: 9–24. doi: 10.1159/000508591 PubMed DOI

Newton RJ, Griffin LE, Bowles KM, Meile C, Gifford S, Givens CE, et al. Genome characteristics of a generalist marine bacterial lineage. The ISME Journal. 2010;4: 784–798. doi: 10.1038/ismej.2009.150 PubMed DOI

Belas R, Horikawa E, Aizawa S-I, Suvanasuthi R. Genetic Determinants of Silicibacter sp. TM1040 Motility. Journal of Bacteriology. 2009;191: 4502–4512. doi: 10.1128/jb.00429-09 PubMed DOI PMC

Sule P, Belas R. A Novel Inducer of Roseobacter Motility Is Also a Disruptor of Algal Symbiosis. Journal of Bacteriology. 2013;195: 637–646. doi: 10.1128/jb.01777-12 PubMed DOI PMC

Komoriya K, Shibano N, Higano T, Azuma N, Yamaguchi S, Aizawa S-I. Flagellar proteins and type III-exported virulence factors are the predominant proteins secreted into the culture media of Salmonella typhimurium. Molecular Microbiology. 1999;34: 767–779. doi: 10.1046/j.1365-2958.1999.01639.x PubMed DOI

Römling U, Galperin MY, Gomelsky M. Cyclic di-GMP: the First 25 Years of a Universal Bacterial Second Messenger. Microbiology and Molecular Biology Reviews. 2013;77: 1–52. doi: 10.1128/mmbr.00043-12 PubMed DOI PMC

Tomasch J, Wang H, Hall AT, Patzelt D, Preusse M, Petersen J, et al. Packaging of Dinoroseobacter shibae DNA into gene transfer agent particles is not random. Genome Biology and Evolution. 2018;10: 359–369. doi: 10.1093/gbe/evy005 PubMed DOI PMC

Craske MW, Wilson JS, Fogg PCM. Gene transfer agents: structural and functional properties of domesticated viruses. Trends in Microbiology. 2024;32: 1200–1211. doi: 10.1016/j.tim.2024.05.002 PubMed DOI

Wang H, Ziesche L, Frank O, Michael V, Martin M, Petersen J, et al. The CtrA phosphorelay integrates differentiation and communication in the marine alphaproteobacterium Dinoroseobacter shibae. BMC Genomics. 2014;15: 130. doi: 10.1186/1471-2164-15-130 PubMed DOI PMC

Wu J, Ohta N, Zhao J-L, Newton A. A novel bacterial tyrosine kinase essential for cell division and differentiation. Proceedings of the National Academy of Sciences. 1999;96: 13068–13073. doi: 10.1073/pnas.96.23.13068 PubMed DOI PMC

Mercer RG, Lang AS. Identification of a predicted partner-switching system that affects production of the gene transfer agent RcGTA and stationary phase viability in Rhodobacter capsulatus. BMC Microbiol. 2014;14: 71. doi: 10.1186/1471-2180-14-71 PubMed DOI PMC

Fogg PCM. Identification and characterization of a direct activator of a gene transfer agent. Nat Commun. 2019;10: 595. doi: 10.1038/s41467-019-08526-1 PubMed DOI PMC

Laass S, Kleist S, Bill N, Drüppel K, Kossmehl S, Wöhlbrand L, et al. Gene Regulatory and Metabolic Adaptation Processes of PubMed DOI PMC

Poggio S, Abreu-Goodger C, Fabela S, Osorio A, Dreyfus G, Vinuesa P, et al. A Complete Set of Flagellar Genes Acquired by Horizontal Transfer Coexists with the Endogenous Flagellar System in Rhodobacter sphaeroides. Journal of Bacteriology. 2007;189: 3208–3216. doi: 10.1128/jb.01681-06 PubMed DOI PMC

Petersen J, Brinkmann H, Bunk B, Michael V, Päuker O, Pradella S. Think pink: photosynthesis, plasmids and the Roseobacter clade. Environmental Microbiology. 2012;14: 2661–2672. doi: 10.1111/j.1462-2920.2012.02806.x PubMed DOI

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. doi: 10.1038/s41396-018-0150-9 PubMed DOI PMC

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. doi: 10.1128/mSystems.00358-19 PubMed DOI PMC

Petersen J, Vollmers J, Ringel V, Brinkmann H, Ellebrandt-Sperling C, Spröer C, et al. A marine plasmid hitchhiking vast phylogenetic and geographic distances. Proceedings of the National Academy of Sciences. 2019;116: 20568–20573. doi: 10.1073/pnas.1905878116 PubMed DOI PMC

Birmes L, Freese HM, Petersen J. RepC_soli: a novel promiscuous plasmid type of Rhodobacteraceae mediates horizontal transfer of antibiotic resistances in the ocean. Environmental Microbiology. 2021;23: 5395–5411. doi: 10.1111/1462-2920.15380 PubMed DOI

Norris V, Madsen MS. Autocatalytic Gene Expression OccursviaTransertion and Membrane Domain Formation and Underlies Differentiation in Bacteria: A Model. Journal of Molecular Biology. 1995;253: 739–748. doi: 10.1006/jmbi.1995.0587 PubMed DOI

Halte M, Andrianova EP, Goosmann C, Chevance FFV, Hughes KT, Zhulin IB, et al. FlhE functions as a chaperone to prevent formation of periplasmic flagella in Gram-negative bacteria. Nat Commun. 2024;15: 5921. doi: 10.1038/s41467-024-50278-0 PubMed DOI PMC

Beyersmann PG, Tomasch J, Son K, Stocker R, Göker M, Wagner-Döbler I, et al. Dual function of tropodithietic acid as antibiotic and signaling molecule in global gene regulation of the probiotic bacterium Phaeobacter inhibens. Sci Rep. 2017;7: 730. doi: 10.1038/s41598-017-00784-7 PubMed DOI PMC

Patzelt D, Wang H, Buchholz I, Rohde M, Gröbe L, Pradella S, et al. You are what you talk: quorum sensing induces individual morphologies and cell division modes in Dinoroseobacter shibae. ISME J. 2013;7: 2274–2286. doi: 10.1038/ismej.2013.107 PubMed DOI PMC

Peña-Castillo L, Mercer RG, Gurinovich A, Callister SJ, Wright AT, Westbye AB, et al. Gene co-expression network analysis in Rhodobacter capsulatus and application to comparative expression analysis of Rhodobacter sphaeroides. BMC Genomics. 2014;15: 730. doi: 10.1186/1471-2164-15-730 PubMed DOI PMC

Koppenhöfer S, Lang AS. Interactions among Redox Regulators and the CtrA Phosphorelay in Dinoroseobacter shibae and Rhodobacter capsulatus. Microorganisms. 2020;8: 562. doi: 10.3390/microorganisms8040562 PubMed DOI PMC

Greene SE, Brilli M, Biondi EG, Komeili A. Analysis of the CtrA Pathway in Magnetospirillum Reveals an Ancestral Role in Motility in Alphaproteobacteria. Journal of Bacteriology. 2012;194: 2973–2986. doi: 10.1128/jb.00170-12 PubMed DOI PMC

Tomasch J, Koppenhöfer S, Lang AS. Connection Between Chromosomal Location and Function of CtrA Phosphorelay Genes in Alphaproteobacteria. Front Microbiol. 2021;12. doi: 10.3389/fmicb.2021.662907 PubMed DOI PMC

Vega-Baray B, Domenzain C, Rivera A, Alfaro-López R, Gómez-César E, Poggio S, et al. The Flagellar Set Fla2 in Rhodobacter sphaeroides Is Controlled by the CckA Pathway and Is Repressed by Organic Acids and the Expression of Fla1. Journal of Bacteriology. 2015;197: 833–847. doi: 10.1128/jb.02429-14 PubMed DOI PMC

Hernández-Valle J, Sanchez-Flores A, Poggio S, Dreyfus G, Camarena L. The CtrA Regulon of Rhodobacter sphaeroides Favors Adaptation to a Particular Lifestyle. Journal of Bacteriology. 2020;202: 10.1128/jb.00678–19. doi: 10.1128/jb.00678-19 PubMed DOI PMC

Lechner M, Findeiß S, Steiner L, Marz M, Stadler PF, Prohaska SJ. Proteinortho: Detection of (Co-)orthologs in large-scale analysis. BMC Bioinformatics. 2011;12: 124. doi: 10.1186/1471-2105-12-124 PubMed DOI PMC

Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics. 2004;5: 113. doi: 10.1186/1471-2105-5-113 PubMed DOI PMC

Castresana J. Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis. Molecular Biology and Evolution. 2000;17: 540–552. doi: 10.1093/oxfordjournals.molbev.a026334 PubMed DOI

Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30: 1312–1313. doi: 10.1093/bioinformatics/btu033 PubMed DOI PMC

Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies. Molecular Biology and Evolution. 2015;32: 268–274. doi: 10.1093/molbev/msu300 PubMed DOI PMC

Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: Improving the Ultrafast Bootstrap Approximation. Molecular Biology and Evolution. 2018;35: 518–522. doi: 10.1093/molbev/msx281 PubMed DOI PMC

Xu S, Li L, Luo X, Chen M, Tang W, Zhan L, et al. Ggtree: A serialized data object for visualization of a phylogenetic tree and annotation data. iMeta. 2022;1: e56. doi: 10.1002/imt2.56 PubMed DOI PMC

Petersen J, Brinkmann H, Pradella S. Diversity and evolution of repABC type plasmids in Rhodobacterales. Environmental Microbiology. 2009;11: 2627–2638. doi: 10.1111/j.1462-2920.2009.01987.x PubMed DOI

Koßmehl S, Wöhlbrand L, Drüppel K, Feenders C, Blasius B, Rabus R. Subcellular protein localization (cell envelope) in Phaeobacter inhibens DSM 17395. PROTEOMICS. 2013;13: 2743–2760. doi: 10.1002/pmic.201300112 PubMed DOI

Wöhlbrand L, Ruppersberg HS, Feenders C, Blasius B, Braun H-P, Rabus R. Analysis of membrane–protein complexes of the marine sulfate reducer Desulfobacula toluolica Tol2 by 1D blue native-PAGE complexome profiling and 2D blue native-/SDS-PAGE. PROTEOMICS. 2016;16: 973–988. doi: 10.1002/pmic.201500360 PubMed DOI

Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9: 357–359. doi: 10.1038/nmeth.1923 PubMed DOI PMC

Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30: 923–930. doi: 10.1093/bioinformatics/btt656 PubMed DOI

Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26: 139–140. doi: 10.1093/bioinformatics/btp616 PubMed DOI PMC

Perez-Riverol Y, Bandla C, Kundu DJ, Kamatchinathan S, Bai J, Hewapathirana S, et al. The PRIDE database at 20 years: 2025 update. Nucleic Acids Research. 2025;53: D543–D553. doi: 10.1093/nar/gkae1011 PubMed DOI PMC

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...