The Biogeochemistry of Marine Polysaccharides: Sources, Inventories, and Bacterial Drivers of the Carbohydrate Cycle

Annual Review of Marine Science, Journal Year: 2020, Volume and Issue: 13(1), P. 81 - 108

Published: July 29, 2020

Polysaccharides are major components of macroalgal and phytoplankton biomass constitute a large fraction the organic matter produced degraded in ocean. Until recently, however, our knowledge marine polysaccharides was limited due to their great structural complexity, correspondingly complicated enzymatic machinery used by microbial communities degrade them, lack readily applied means isolate andcharacterize detail. Advances carbohydrate chemistry, bioinformatics, molecular ecology, microbiology have led new insights into structures polysaccharides, which they bacteria, ecology polysaccharide production decomposition. Here, we survey current knowledge, discuss recent advances, present conceptual model linking complexity abundance microbially driven mechanisms processing. We conclude highlighting specific future research foci that will shed light on this central but poorly characterized component carbon cycle.

Language: Английский

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Comparison of Two 16S rRNA Primers (V3–V4 and V4–V5) for Studies of Arctic Microbial Communities

Frontiers in Microbiology, Journal Year: 2021, Volume and Issue: 12

Published: Feb. 16, 2021

Microbial communities of the Arctic Ocean are poorly characterized in comparison to other aquatic environments as their horizontal, vertical, and temporal turnover. Yet, recent studies showed that marine ecosystem harbors unique microbial community members adapted harsh environmental conditions, such near-freezing temperatures extreme seasonality. The gene for small ribosomal subunit (16S rRNA) is commonly used study taxonomic composition natural environment. Several primer sets this marker have been extensively tested across various sample sets, but these typically originated from low-latitude environments. An explicit evaluation primer-set performances representing currently lacking. To select a suitable set studying microbiomes habitats (sea ice, surface water, snow, deep ocean basin, deep-sea sediment), we conducted performance between two widely targeting different hypervariable regions 16S rRNA (V3-V4 V4-V5). We observed both were highly similar total down genus rank, which was also confirmed independently by subgroup-specific catalyzed reporter deposition-fluorescence

Language: Английский

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Dissolved storage glycans shaped the community composition of abundant bacterioplankton clades during a North Sea spring phytoplankton bloom

Microbiome, Journal Year: 2023, Volume and Issue: 11(1)

Published: April 17, 2023

Abstract Background Blooms of marine microalgae play a pivotal role in global carbon cycling. Such blooms entail successive specialized clades planktonic bacteria that collectively remineralize gigatons algal biomass on scale. This is largely composed distinct polysaccharides, and the microbial decomposition these polysaccharides therefore process prime importance. Results In 2020, we sampled complete biphasic spring bloom German Bight over 90-day period. Bacterioplankton metagenomes from 30 time points allowed reconstruction 251 metagenome-assembled genomes (MAGs). Corresponding metatranscriptomes highlighted 50 particularly active MAGs most abundant clades, including many polysaccharide degraders. Saccharide measurements together with bacterial utilization loci (PUL) expression data identified β -glucans (diatom laminarin) α as prominent actively metabolized dissolved substrates. Both substrates were consumed throughout bloom, -glucan PUL peaking at beginning second phase shortly after peak flagellate nadir total cell counts. Conclusions We show amounts composition particular storage have pronounced influence bacterioplankton members during phytoplankton blooms, some which compete for similar niches. hypothesize besides release glycans, also recycling glycans result increased mortality can significant blooms.

Language: Английский

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Particle-attached bacteria act as gatekeepers in the decomposition of complex phytoplankton polysaccharides

Microbiome, Journal Year: 2024, Volume and Issue: 12(1)

Published: Feb. 20, 2024

Abstract Background Marine microalgae (phytoplankton) mediate almost half of the worldwide photosynthetic carbon dioxide fixation and therefore play a pivotal role in global cycling, most prominently during massive phytoplankton blooms. Phytoplankton biomass consists considerable proportions polysaccharides, substantial parts which are rapidly remineralized by heterotrophic bacteria. We analyzed diversity, activity, functional potential such polysaccharide-degrading bacteria different size fractions diverse spring bloom at Helgoland Roads (southern North Sea) high temporal resolution using microscopic, physicochemical, biodiversity, metagenome, metaproteome analyses. Results Prominent active 0.2–3 µm free-living clades comprised Aurantivirga , “Formosa”, Cd . Prosiliicoccus, NS4, NS5, Amylibacter Planktomarina SAR11 Ia, SAR92, SAR86, whereas BD1-7, Stappiaceae Nitrincolaceae Methylophagaceae Sulfitobacter NS9, Polaribacter Lentimonas CL500-3, Algibacter Glaciecola dominated 3–10 > 10 particles. Particle-attached were more exhibited dynamic adaptive shifts over time terms taxonomic composition repertoires encoded polysaccharide-targeting enzymes. In total, 305 species-level metagenome-assembled genomes obtained, including 152 particle-attached bacteria, 100 novel for sampling site with 76 representing new species. Compared to they featured on average larger higher polysaccharide utilization loci. The latter predicted target broader spectrum substrates, ranging from readily soluble, simple structured storage polysaccharides (e.g., laminarin, α-glucans) less complex structural, or secreted xylans, cellulose, pectins). particular, poorly soluble was widespread among abundant Conclusions represented only 1% all bloom-associated yet our data suggest that many played gatekeeping solubilization subsequent degradation numerous important classes algal glycans. diversity niches is determining factor proportion can be generally short-lived events.

Language: Английский

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Resource partitioning of phytoplankton metabolites that support bacterial heterotrophy

The ISME Journal, Journal Year: 2020, Volume and Issue: 15(3), P. 762 - 773

Published: Oct. 23, 2020

Abstract The communities of bacteria that assemble around marine microphytoplankton are predictably dominated by Rhodobacterales, Flavobacteriales, and families within the Gammaproteobacteria. Yet whether this consistent ecological pattern reflects result resource-based niche partitioning or resource competition requires better knowledge metabolites linking microbial autotrophs heterotrophs in surface ocean. We characterized molecules targeted for uptake three heterotrophic individually co-cultured with a diatom using two strategies vetted exometabolite pool biological relevance means bacterial activity assays: expression diagnostic genes net drawdown exometabolites, latter detected mass spectrometry nuclear magnetic resonance novel sample preparation approaches. Of more than 36 organic evidence uptake, 53% contained nitrogen (including nucleosides amino acids), 11% were sulfur compounds dihydroxypropanesulfonate dimethysulfoniopropionate), 28% components polysaccharides chrysolaminarin, chitin, alginate). Overlap phytoplankton-derived metabolite use absence was low, only guanosine, proline, N-acetyl-d-glucosamine predicted to be used all three. Exometabolite points key role assembly transforming recent photosynthate.

Language: Английский

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Changing expression patterns of TonB-dependent transporters suggest shifts in polysaccharide consumption over the course of a spring phytoplankton bloom

The ISME Journal, Journal Year: 2021, Volume and Issue: 15(8), P. 2336 - 2350

Published: March 1, 2021

Abstract Algal blooms produce large quantities of organic matter that is subsequently remineralised by bacterial heterotrophs. Polysaccharide a primary component algal biomass. It has been hypothesised individual heterotrophic niches during are in part determined the available polysaccharide substrates present. Measurement expression TonB-dependent transporters, often specific for uptake, might serve as proxy assessing consumption over time. To investigate this, we present here high-resolution metaproteomic and metagenomic datasets from bacterioplankton 2016 spring phytoplankton bloom at Helgoland island southern North Sea, profiles transporters bloom, which demonstrate importance both Gammaproteobacteria Bacteroidetes degraders polysaccharide. were most highly expressed protein class, split approximately evenly between Bacteroidetes, totalling on average 16.7% all detected proteins bloom. About 93% these predicted to take up matter, about 12% target class. Most significantly, observed change substrate specificities time, was not reflected corresponding data. From conclude cell wall-related compounds containing fucose, mannose, xylose mostly utilised later stages, whereas glucose-based storage molecules including laminarin, glycogen, starch used throughout. Quantification could therefore be key understanding marine carbon cycling.

Language: Английский

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Genomic and metabolic adaptations of biofilms to ecological windows of opportunity in glacier-fed streams

Nature Communications, Journal Year: 2022, Volume and Issue: 13(1)

Published: April 20, 2022

In glacier-fed streams, ecological windows of opportunity allow complex microbial biofilms to develop and transiently form the basis food web, thereby controlling key ecosystem processes. Using metagenome-assembled genomes, we unravel strategies that seize this in an otherwise characterized by harsh environmental conditions. We observe a diverse microbiome spanning entire tree life including rich virome. Various co-existing energy acquisition pathways point niches exploitation available resources, likely fostering establishment during opportunity. The wide occurrence rhodopsins, besides chlorophyll, highlights role solar capture these while internal carbon nutrient cycling between photoautotrophs heterotrophs may help overcome constraints imposed oligotrophy habitats. Mechanisms potentially protecting bacteria against low temperatures high UV-radiation are also revealed selective pressure environment is further highlighted phylogenomic analysis differentiating important components stream from other ecosystems. Our findings reveal genomic underpinnings adaptive traits contributing success exploit opportunities which now rapidly changing owing global warming.

Language: Английский

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Highly diverse flavobacterial phages isolated from North Sea spring blooms

The ISME Journal, Journal Year: 2021, Volume and Issue: 16(2), P. 555 - 568

Published: Sept. 2, 2021

Abstract It is generally recognized that phages are a mortality factor for their bacterial hosts. This could be particularly true in spring phytoplankton blooms, which known to closely followed by highly specialized community. We hypothesized modulate these dense heterotrophic bacteria successions following blooms. In this study, we focused on Flavobacteriia, because they main responders during blooms and have an important role the degradation of polysaccharides. A cultivation-based approach was used, obtaining 44 lytic flavobacterial (flavophages), representing twelve new species from two viral realms. Taxonomic analysis allowed us delineate ten phage genera families, nine four, respectively, had no previously cultivated representatives. Genomic predicted various life styles genomic replication strategies. likely eukaryote-associated host habitat reflected gene content some flavophages. Detection cellular metagenomes direct-plating showed part were actively replicating environment 2018 bloom. Furthermore, CRISPR/Cas spacers re-isolation consecutive years suggested that, at least flavophages stable components microbial community North Sea. Together, our results indicate diverse potential respective populations.

Language: Английский

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North Sea spring bloom-associated Gammaproteobacteria fill diverse heterotrophic niches

Environmental Microbiome, Journal Year: 2021, Volume and Issue: 16(1)

Published: Aug. 17, 2021

Abstract Background The planktonic bacterial community associated with spring phytoplankton blooms in the North Sea is responsible for a large amount of carbon turnover an environment characterised by high primary productivity. Individual clades belonging to Gammaproteobacteria have shown similar population dynamics Bacteroidetes species , and are thus assumed fill competing ecological niches. Previous studies generated numbers metagenome assembled genomes metaproteomes from these environments, which can be readily mined identify populations performing potentially important ecosystem functions. In this study we attempt catalogue bloom-associated far attracted less attention than sympatric Alphaproteobacteria . Methods We annotated 120 non-redundant species-representative gammaproteobacterial bloom sampling campaigns covering four years 2010–2012 2016 using combination Prokka PfamScan, further confirmation via BLAST against NCBI-NR. also matched gene annotations 20 previously published those periods plus 2009. Results Metagenome clear capacity polysaccharide degradation dedicated clusters carbohydrate active enzymes were among most abundant during blooms. Many lacked clearly identifiable predicted substrates, although abundantly expressed loci uptake molecules identified metaproteomes. While larger biopolymers, sources reduced following algal blooms, likely main energy source, some specialised smaller organic compounds. Their substrates range amino acids, monosaccharides, DMSP, expected, such as terpenoids, aromatics biphenyls, well many ‘unknowns’. particular uncover much greater breadth apparent methylotrophic capability heretofore identified, present several order level without cultivated representatives. Conclusions Large today publicly available, containing wealth accessible information. Here variety metabolisms interest, include diverse potential heterotrophic niches Features here could fertile ground future experimental studies.

Language: Английский

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Structures and functions of algal glycans shape their capacity to sequester carbon in the ocean

Current Opinion in Chemical Biology, Journal Year: 2022, Volume and Issue: 71, P. 102204 - 102204

Published: Sept. 22, 2022

Algae synthesise structurally complex glycans to build a protective barrier, the extracellular matrix. One function of matrix is slow down microorganisms that try enzymatically enter living algae and degrade convert their organic carbon back dioxide. We propose lock up in ocean by controlling degradation bacteria other microbes not only while are alive, but also after death. Data revised this review shows accumulation algal underscoring challenge face breach glycan barrier with carbohydrate active enzymes. Briefly we update on methods required certify uncertain magnitude unknown molecular causes glycan-controlled sequestration changing ocean.

Language: Английский

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