Particle-attached bacteria act as gatekeepers in the decomposition of complex phytoplankton polysaccharides.
Algal bloom
Algal polysaccharide
Bacterioplankton
Bacteroidota
Carbohydrate-active enzyme
Carbon budget
Carbon cycle
Free-living bacteria
Helgoland Roads LTER
Marine microbes
Particle-attached bacteria
Particulate organic matter
Polysaccharide utilization locus
Journal
Microbiome
ISSN: 2049-2618
Titre abrégé: Microbiome
Pays: England
ID NLM: 101615147
Informations de publication
Date de publication:
20 Feb 2024
20 Feb 2024
Historique:
received:
07
11
2023
accepted:
04
01
2024
medline:
20
2
2024
pubmed:
20
2
2024
entrez:
19
2
2024
Statut:
epublish
Résumé
Marine microalgae (phytoplankton) mediate almost half of the worldwide photosynthetic carbon dioxide fixation and therefore play a pivotal role in global carbon cycling, most prominently during massive phytoplankton blooms. Phytoplankton biomass consists of considerable proportions of polysaccharides, substantial parts of which are rapidly remineralized by heterotrophic bacteria. We analyzed the diversity, activity, and functional potential of such polysaccharide-degrading bacteria in different size fractions during a diverse spring phytoplankton bloom at Helgoland Roads (southern North Sea) at high temporal resolution using microscopic, physicochemical, biodiversity, metagenome, and metaproteome analyses. Prominent active 0.2-3 µm free-living clades comprised Aurantivirga, "Formosa", Cd. Prosiliicoccus, NS4, NS5, Amylibacter, Planktomarina, SAR11 Ia, SAR92, and SAR86, whereas BD1-7, Stappiaceae, Nitrincolaceae, Methylophagaceae, Sulfitobacter, NS9, Polaribacter, Lentimonas, CL500-3, Algibacter, and Glaciecola dominated 3-10 µm and > 10 µm particles. Particle-attached bacteria were more diverse and exhibited more dynamic adaptive shifts over time in terms of taxonomic composition and repertoires of encoded polysaccharide-targeting enzymes. In total, 305 species-level metagenome-assembled genomes were obtained, including 152 particle-attached bacteria, 100 of which were novel for the sampling site with 76 representing new species. Compared to free-living bacteria, they featured on average larger metagenome-assembled genomes with higher proportions of polysaccharide utilization loci. The latter were predicted to target a broader spectrum of polysaccharide substrates, ranging from readily soluble, simple structured storage polysaccharides (e.g., laminarin, α-glucans) to less soluble, complex structural, or secreted polysaccharides (e.g., xylans, cellulose, pectins). In particular, the potential to target poorly soluble or complex polysaccharides was more widespread among abundant and active particle-attached bacteria. Particle-attached bacteria represented only 1% of all bloom-associated bacteria, yet our data suggest that many abundant active clades played a pivotal gatekeeping role in the solubilization and subsequent degradation of numerous important classes of algal glycans. The high diversity of polysaccharide niches among the most active particle-attached clades therefore is a determining factor for the proportion of algal polysaccharides that can be rapidly remineralized during generally short-lived phytoplankton bloom events. Video Abstract.
Sections du résumé
BACKGROUND
BACKGROUND
Marine microalgae (phytoplankton) mediate almost half of the worldwide photosynthetic carbon dioxide fixation and therefore play a pivotal role in global carbon cycling, most prominently during massive phytoplankton blooms. Phytoplankton biomass consists of considerable proportions of polysaccharides, substantial parts of which are rapidly remineralized by heterotrophic bacteria. We analyzed the diversity, activity, and functional potential of such polysaccharide-degrading bacteria in different size fractions during a diverse spring phytoplankton bloom at Helgoland Roads (southern North Sea) at high temporal resolution using microscopic, physicochemical, biodiversity, metagenome, and metaproteome analyses.
RESULTS
RESULTS
Prominent active 0.2-3 µm free-living clades comprised Aurantivirga, "Formosa", Cd. Prosiliicoccus, NS4, NS5, Amylibacter, Planktomarina, SAR11 Ia, SAR92, and SAR86, whereas BD1-7, Stappiaceae, Nitrincolaceae, Methylophagaceae, Sulfitobacter, NS9, Polaribacter, Lentimonas, CL500-3, Algibacter, and Glaciecola dominated 3-10 µm and > 10 µm particles. Particle-attached bacteria were more diverse and exhibited more dynamic adaptive shifts over time in terms of taxonomic composition and repertoires of encoded polysaccharide-targeting enzymes. In total, 305 species-level metagenome-assembled genomes were obtained, including 152 particle-attached bacteria, 100 of which were novel for the sampling site with 76 representing new species. Compared to free-living bacteria, they featured on average larger metagenome-assembled genomes with higher proportions of polysaccharide utilization loci. The latter were predicted to target a broader spectrum of polysaccharide substrates, ranging from readily soluble, simple structured storage polysaccharides (e.g., laminarin, α-glucans) to less soluble, complex structural, or secreted polysaccharides (e.g., xylans, cellulose, pectins). In particular, the potential to target poorly soluble or complex polysaccharides was more widespread among abundant and active particle-attached bacteria.
CONCLUSIONS
CONCLUSIONS
Particle-attached bacteria represented only 1% of all bloom-associated bacteria, yet our data suggest that many abundant active clades played a pivotal gatekeeping role in the solubilization and subsequent degradation of numerous important classes of algal glycans. The high diversity of polysaccharide niches among the most active particle-attached clades therefore is a determining factor for the proportion of algal polysaccharides that can be rapidly remineralized during generally short-lived phytoplankton bloom events. Video Abstract.
Identifiants
pubmed: 38374154
doi: 10.1186/s40168-024-01757-5
pii: 10.1186/s40168-024-01757-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
32Subventions
Organisme : Deutsche Forschungsgemeinschaft,Germany
ID : AM 73/9-3
Organisme : Deutsche Forschungsgemeinschaft,Germany
ID : SCHW 595/10-3
Organisme : Deutsche Forschungsgemeinschaft,Germany
ID : TE 813/2-3
Organisme : Deutsche Forschungsgemeinschaft,Germany
ID : RI 969/9-2
Organisme : Deutsche Forschungsgemeinschaft,Germany
ID : BE 3869/4-3
Organisme : Deutsche Forschungsgemeinschaft,Germany
ID : SCHW 595/11-3
Organisme : Deutsche Forschungsgemeinschaft,Germany
ID : FU 627/2-3
Organisme : Deutsche Forschungsgemeinschaft,Germany
ID : RI 969/9-2
Organisme : Deutsche Forschungsgemeinschaft,Germany
ID : TE 813/2-3
Organisme : Deutsche Forschungsgemeinschaft,Germany
ID : AM 73/9-3
Organisme : Biological Station Helgoland, Alfred Wegener Institute, Helmholtz Center for Polar and Marine Research
ID : AWI_BAH_o 1
Organisme : Biological Station Helgoland, Alfred Wegener Institute, Helmholtz Center for Polar and Marine Research
ID : AWI_BAH_o 1
Informations de copyright
© 2024. The Author(s).
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