Evolutionary history and association with seaweeds shape the genomes and metabolisms of marine bacteria
ABSTRACT Seaweeds harbor a rich diversity of bacteria, providing them with metabolic resources and a surface for attachment and biofilm development. The host’s unique environment potentially shapes the bacterial genomes and promotes adaptations for a symbiotic lifestyle. To investigate whether the g...
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American Society for Microbiology
2025-06-01
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| Online Access: | https://journals.asm.org/doi/10.1128/msphere.00996-24 |
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| author | Catherine A. Pfister Johanna Berlinghof Maximiliana Bogan Ulisse Cardini Angélique Gobet Pauline Hamon-Giraud Jessica Hart Natalia Jimenez Anne Siegel Emma Stanfield Marine Vallet Catherine Leblanc Coralie Rousseau François Thomas Willem Stock Simon M. Dittami |
| author_facet | Catherine A. Pfister Johanna Berlinghof Maximiliana Bogan Ulisse Cardini Angélique Gobet Pauline Hamon-Giraud Jessica Hart Natalia Jimenez Anne Siegel Emma Stanfield Marine Vallet Catherine Leblanc Coralie Rousseau François Thomas Willem Stock Simon M. Dittami |
| author_sort | Catherine A. Pfister |
| collection | DOAJ |
| description | ABSTRACT Seaweeds harbor a rich diversity of bacteria, providing them with metabolic resources and a surface for attachment and biofilm development. The host’s unique environment potentially shapes the bacterial genomes and promotes adaptations for a symbiotic lifestyle. To investigate whether the genomes of seaweed-associated bacteria are genetically and metabolically distinct from their close free-living relatives in seawater, we compared both the seaweed-associated and free-living counterparts of 72 bacterial genera across 16 seaweed hosts using whole-genome sequences or high-quality metagenome-assembled genomes. While taxonomic affiliation strongly influenced genome characteristics such as GC content, gene number, and size, host association had a lower effect overall. A reduced genome size was suggested only in Nereocystis luetkeana-associated microbes, while only Ascophyllum nodosum-associated bacteria had an increased GC content. Metabolic adaptations were indicated from the genomes of seaweed-associated bacteria, including enriched pathways for B vitamin production, complex carbohydrate utilization, and amino acid biosynthesis. In particular, Flavobacteriia showed the most pronounced differences between host-associated and free-living strains. We further hypothesized that bacteria associated with seaweed might have evolved to complement their host’s metabolism and tested this inference by analyzing the genomes of both the seaweed Ectocarpus subulatus and its 28 bacterial associates but found no evidence for such complementarity. Our analyses of 72 paired bacterial genomes highlighted significant metabolic differences in seaweed-associated strains with implications for carbon, nitrogen, and sulfur cycling in the coastal ocean.IMPORTANCEWe hypothesized that the unique environment of seaweeds in coastal oceans shapes bacterial genomes and promotes a symbiotic lifestyle. We compared the genomes of bacteria isolated from seaweed with bacteria from the same genus found free-living in seawater. For genome features that included the number of genes, the size of the genome, and the GC content, taxonomy was of greater importance than bacterial lifestyle. When we compared metabolic abilities, we again found a strong effect of taxonomy in determining metabolism. Although several metabolic pathways differed between free-living and host-associated bacteria, this was especially prominent for Flavobacteriia in the phylum Bacteroidota. Notably, bacteria living on seaweeds had an increased occurrence of genes for B vitamin synthesis, complex carbohydrate use, and nitrogen uptake, indicating that bacterial genomes reflect both their evolutionary history and the current environment they inhabit. |
| format | Article |
| id | doaj-art-5faaffe40b4140ad87f5e8af9b433c07 |
| institution | Kabale University |
| issn | 2379-5042 |
| language | English |
| publishDate | 2025-06-01 |
| publisher | American Society for Microbiology |
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| spelling | doaj-art-5faaffe40b4140ad87f5e8af9b433c072025-08-20T03:26:33ZengAmerican Society for MicrobiologymSphere2379-50422025-06-0110610.1128/msphere.00996-24Evolutionary history and association with seaweeds shape the genomes and metabolisms of marine bacteriaCatherine A. Pfister0Johanna Berlinghof1Maximiliana Bogan2Ulisse Cardini3Angélique Gobet4Pauline Hamon-Giraud5Jessica Hart6Natalia Jimenez7Anne Siegel8Emma Stanfield9Marine Vallet10Catherine Leblanc11Coralie Rousseau12François Thomas13Willem Stock14Simon M. Dittami15Department of Ecology & Evolution, The University of Chicago, Chicago, Illinois, USAGenoa Marine Center, Stazione Zoologica Anton Dohrn, Genoa, ItalyDepartment of Ecology & Evolution, The University of Chicago, Chicago, Illinois, USAGenoa Marine Center, Stazione Zoologica Anton Dohrn, Genoa, ItalyMARBEC, Univ Montpellier, CNRS, Ifremer, IRD, Sète, FranceCNRS, Inria, IRISA (UMR 6074), University of Rennes, Rennes, Brittany, FranceDepartment of Ecology & Evolution, The University of Chicago, Chicago, Illinois, USAInstitute for Biological and Medical Engineering, Schools of Engineering, Medicine and Biological Sciences, Pontificia Universidad Católica de Chile, Santiago, ChileCNRS, Inria, IRISA (UMR 6074), University of Rennes, Rennes, Brittany, FranceDepartment of Ecology & Evolution, The University of Chicago, Chicago, Illinois, USAInstitute for Inorganic and Analytical Chemistry, Friedrich Schiller University Jena, Jena, Thuringia, GermanyIntegrative Biology of Marine Models (LBI2M, UMR 8227), CNRS, Station Biologique de Roscoff (SBR), Sorbonne University, Roscoff, Brittany, FranceIntegrative Biology of Marine Models (LBI2M, UMR 8227), CNRS, Station Biologique de Roscoff (SBR), Sorbonne University, Roscoff, Brittany, FranceIntegrative Biology of Marine Models (LBI2M, UMR 8227), CNRS, Station Biologique de Roscoff (SBR), Sorbonne University, Roscoff, Brittany, FrancePhycology Research Group, Department of Biology, Ghent University, Ghent, Flanders, BelgiumIntegrative Biology of Marine Models (LBI2M, UMR 8227), CNRS, Station Biologique de Roscoff (SBR), Sorbonne University, Roscoff, Brittany, FranceABSTRACT Seaweeds harbor a rich diversity of bacteria, providing them with metabolic resources and a surface for attachment and biofilm development. The host’s unique environment potentially shapes the bacterial genomes and promotes adaptations for a symbiotic lifestyle. To investigate whether the genomes of seaweed-associated bacteria are genetically and metabolically distinct from their close free-living relatives in seawater, we compared both the seaweed-associated and free-living counterparts of 72 bacterial genera across 16 seaweed hosts using whole-genome sequences or high-quality metagenome-assembled genomes. While taxonomic affiliation strongly influenced genome characteristics such as GC content, gene number, and size, host association had a lower effect overall. A reduced genome size was suggested only in Nereocystis luetkeana-associated microbes, while only Ascophyllum nodosum-associated bacteria had an increased GC content. Metabolic adaptations were indicated from the genomes of seaweed-associated bacteria, including enriched pathways for B vitamin production, complex carbohydrate utilization, and amino acid biosynthesis. In particular, Flavobacteriia showed the most pronounced differences between host-associated and free-living strains. We further hypothesized that bacteria associated with seaweed might have evolved to complement their host’s metabolism and tested this inference by analyzing the genomes of both the seaweed Ectocarpus subulatus and its 28 bacterial associates but found no evidence for such complementarity. Our analyses of 72 paired bacterial genomes highlighted significant metabolic differences in seaweed-associated strains with implications for carbon, nitrogen, and sulfur cycling in the coastal ocean.IMPORTANCEWe hypothesized that the unique environment of seaweeds in coastal oceans shapes bacterial genomes and promotes a symbiotic lifestyle. We compared the genomes of bacteria isolated from seaweed with bacteria from the same genus found free-living in seawater. For genome features that included the number of genes, the size of the genome, and the GC content, taxonomy was of greater importance than bacterial lifestyle. When we compared metabolic abilities, we again found a strong effect of taxonomy in determining metabolism. Although several metabolic pathways differed between free-living and host-associated bacteria, this was especially prominent for Flavobacteriia in the phylum Bacteroidota. Notably, bacteria living on seaweeds had an increased occurrence of genes for B vitamin synthesis, complex carbohydrate use, and nitrogen uptake, indicating that bacterial genomes reflect both their evolutionary history and the current environment they inhabit.https://journals.asm.org/doi/10.1128/msphere.00996-24host-microbenonhuman microbiomemarine bacteriamicrobial metabolismbacterial genomes |
| spellingShingle | Catherine A. Pfister Johanna Berlinghof Maximiliana Bogan Ulisse Cardini Angélique Gobet Pauline Hamon-Giraud Jessica Hart Natalia Jimenez Anne Siegel Emma Stanfield Marine Vallet Catherine Leblanc Coralie Rousseau François Thomas Willem Stock Simon M. Dittami Evolutionary history and association with seaweeds shape the genomes and metabolisms of marine bacteria mSphere host-microbe nonhuman microbiome marine bacteria microbial metabolism bacterial genomes |
| title | Evolutionary history and association with seaweeds shape the genomes and metabolisms of marine bacteria |
| title_full | Evolutionary history and association with seaweeds shape the genomes and metabolisms of marine bacteria |
| title_fullStr | Evolutionary history and association with seaweeds shape the genomes and metabolisms of marine bacteria |
| title_full_unstemmed | Evolutionary history and association with seaweeds shape the genomes and metabolisms of marine bacteria |
| title_short | Evolutionary history and association with seaweeds shape the genomes and metabolisms of marine bacteria |
| title_sort | evolutionary history and association with seaweeds shape the genomes and metabolisms of marine bacteria |
| topic | host-microbe nonhuman microbiome marine bacteria microbial metabolism bacterial genomes |
| url | https://journals.asm.org/doi/10.1128/msphere.00996-24 |
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