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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Low-level resource partitioning supports coexistence among functionally redundant bacteria during successional dynamics

The ISME Journal, Journal Year: 2024, Volume and Issue: 18(1)

Published: Jan. 1, 2024

Abstract Members of microbial communities can substantially overlap in substrate use. However, what enables functionally redundant microorganisms to coassemble or even stably coexist remains poorly understood. Here, we show that during unstable successional dynamics on complex, natural organic matter, bacteria by partitioning low-concentration substrates though they compete for one simple, dominant substrate. We allowed ocean self-assemble leachates the brown seaweed Fucus vesiculosus and then analyzed competition among 10 taxonomically diverse isolates representing two distinct stages succession. All, but isolates, exhibited an average 90% ± 6% pairwise resource use, functional redundancy from same assembly stage was higher than between stages, leading us construct a simpler four-isolate community with each early late stages. found that, although short-term F. leachate dependent initial isolate ratios, long term, four leachate, albeit some strains at low abundance. therefore explored potential nonredundant use genomic content analysis RNA expression patterns. This revealed mainly differed peripheral metabolic pathways, such as ability degrade pyrimidine, leucine, tyrosine, well aromatic substrates. These results highlight importance fine-scale differences strategies supporting frequently observed coexistence large numbers rare organisms microbiomes.

Language: Английский

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Quorum Sensing Regulates Bacterial Processes That Play a Major Role in Marine Biogeochemical Cycles

Frontiers in Marine Science, Journal Year: 2022, Volume and Issue: 9

Published: Feb. 2, 2022

Bacteria play a crucial role in marine biogeochemistry by releasing, consuming and transforming organic matter. Far from being isolated entities, bacteria are involved numerous cell–cell interactions. Among such interactions, quorum sensing (QS) allows to operate unison, synchronizing their actions through chemical communication. This review aims explore synthesize our current knowledge of the involvement QS regulation bacterial processes that ultimately impact biogeochemical cycles. We first describe principles communication renewed interest its study environments. Second, we highlight microniches where is most likely occur due high densities also hotspots bacterially mediated transformations. Many groups colonizing these harbor various systems. Thereafter, relevant QS-regulated environments, building on research performed both complex assemblages bacteria. pathways have been shown directly regulate matter degradation, carbon allocation nutrient acquisition but structure community composition mediating colonization microbial Finally, discuss limitations future perspectives better characterize link between expression mediation The picture drawn this highlights as one pivotal mechanisms impacting functions oceans, paving way for constrain

Language: Английский

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Increased microbial and substrate complexity result in higher molecular diversity of the dissolved organic matter pool

Limnology and Oceanography, Journal Year: 2022, Volume and Issue: 67(11), P. 2360 - 2373

Published: Aug. 27, 2022

Abstract Marine dissolved organic matter (DOM) represents one of the largest reduced carbon pools on Earth. Diverse microbial metabolic activities play important roles in shaping this pool. However, links between changing DOM substrates and communities its influence produced remain poorly understood. In study, we investigated how addition with different complexity (glucose, laminarin, Synechococcus ‐derived DOM) impacted production new by an individual opportunist Alteromonas strain a coastal natural community. Our experiments reveal that was more than substrate molecular composition DOM. Furthermore, our results showed played larger role compositions concentrations inorganic nutrients. Combined network analysis revealed complex resulted higher diversity DOM, sustained diversity, maintained diverse association molecules. Overall, present study indicate contributes to vice versa, highlighting importance microbial–substrate interactions marine

Language: Английский

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Atlantic water influx and sea-ice cover drive taxonomic and functional shifts in Arctic marine bacterial communities

The ISME Journal, Journal Year: 2023, Volume and Issue: 17(10), P. 1612 - 1625

Published: July 8, 2023

The Arctic Ocean is experiencing unprecedented changes because of climate warming, necessitating detailed analyses on the ecology and dynamics biological communities to understand current future ecosystem shifts. Here, we generated a four-year, high-resolution amplicon dataset along with one annual cycle PacBio HiFi read metagenomes from East Greenland Current (EGC), combined this datasets spanning different spatiotemporal scales (Tara MOSAiC) assess impact Atlantic water influx sea-ice cover bacterial in Ocean. Densely ice-covered polar waters harboured temporally stable, resident microbiome. reduced resulted dominance seasonally fluctuating populations, resembling process "replacement" through advection, mixing environmental sorting. We identified signature populations distinct regimes, including night high-ice cover, assessed their ecological roles. Dynamics were consistent across wider Arctic; e.g. those associated dense ice winter EGC abundant central winter. Population- community-level revealed metabolic distinctions between bacteria affiliated conditions; former increased potential use bacterial- terrestrial-derived substrates or inorganic compounds. Our evidence over provides novel insights into indicates progressing Biological Atlantification warming Ocean, consequences for food webs biogeochemical cycles.

Language: Английский

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Inherent tendency of Synechococcus and heterotrophic bacteria for mutualism on long-term coexistence despite environmental interference

Science Advances, Journal Year: 2022, Volume and Issue: 8(39)

Published: Sept. 30, 2022

Mutualism between Synechococcus and heterotrophic bacteria has been found to support their prolonged survival in nutrient-depleted conditions. However, environmental interference on the fate of mutualism is not understood. Here, we show that exogenous nutrients disrupt established mutualism. Once were exhausted, gradually reestablished metabolic during 450 days culture, which revived unhealthy cells. Using metagenomics, metatranscriptomics, 15N tracer method, reveal associated bacterial nitrogen fixation triggered reestablishment revival health. During this process, community structure functions underwent tremendous adjustments achieve driving effect, a cogeneration nitrogen, phosphorus, iron, vitamin by sustained Synechococcus's healthy growth. Our findings suggest may have an inherent tendency toward despite interference. This exhibit coevolutionary adaptations nutrient-deficient environments.

Language: Английский

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Carbohydrates and carbohydrate degradation gene abundance and transcription in Atlantic waters of the Arctic

ISME Communications, Journal Year: 2023, Volume and Issue: 3(1)

Published: Dec. 1, 2023

Carbohydrates are chemically and structurally diverse, represent a substantial fraction of marine organic matter key substrates for heterotrophic microbes. Studies on carbohydrate utilisation by microbes have been centred phytoplankton blooms in temperate regions, while far less is known from high-latitude waters during later seasonal stages. Here, we combine glycan microarrays analytical chromatography with metagenomics metatranscriptomics to show the spatial heterogeneity distribution potential Atlantic Arctic. The composition abundance monomers structures POM varied location depth. Complex fucose-containing sulfated polysaccharides, accumulate ocean, were consistently detected, more labile β-1,3-glucan exhibited patchy distribution. Through 'omics analysis, identify variations transcription degradation-related genes across samples at community population level. populations contributing most taxonomically related those as primary responders degraders ecosystems, such NS4 Marine Group Formosa. unique profiles these suggest distinct substrate potentials, predicted targets corresponding identified same sampling sites. By combining cutting-edge technologies protocols, provide insights into component carbon cycle Arctic late summer present high-quality dataset that will be great value future comparative analyses.

Language: Английский

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Polymeric carbohydrates utilization separates microbiomes into niches: insights into the diversity of microbial carbohydrate-active enzymes in the inner shelf of the Pearl River Estuary, China

Frontiers in Microbiology, Journal Year: 2023, Volume and Issue: 14

Published: June 21, 2023

Polymeric carbohydrates are abundant and their recycling by microbes is a key process of the ocean carbon cycle. A deeper analysis carbohydrate-active enzymes (CAZymes) can offer window into mechanisms microbial communities to degrade in ocean. In this study, metagenomic genes encoding CAZymes sugar transporter systems were predicted assess glycan niches functional potentials utilization inner shelf Pearl River Estuary (PRE). The gene compositions significantly different between free-living (0.2–3 μm, FL) particle-associated (>3 PA) bacteria water column surface sediments, reflecting niche separation on size fraction selective degradation depth. Proteobacteria Bacteroidota had highest abundance width genes, respectively. At genus level, Alteromonas (Gammaproteobacteria) exhibited greatest marked high periplasmic protein TonB members major facilitator superfamily (MFS). increasing contribution transporters for bottom contrasted metabolism tightly related with particulate (pectin, alginate, starch, lignin-cellulose, chitin, peptidoglycan) rather than ambient-water DOC. Candidatus Pelagibacter (Alphaproteobacteria) narrow was primarily preferred nitrogen-containing carbohydrates, while ABC (ATP binding cassette) supported scavenging mode carbohydrate assimilation. Planctomycetota, Verrucomicrobiota, similar potential consumption main component transparent exopolymer particles (sulfated fucose rhamnose containing polysaccharide sulfated-N-glycan), developing considerable overlap among these taxa. most as well widest bacterial taxa implied roles organic utilization, degree composition importantly influenced coastal waters PRE. These findings expand current understanding biotransformation, underlying size-fractionated near estuarine system.

Language: Английский

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The Bacterial Microbiome of the Coral Skeleton Algal Symbiont Ostreobium Shows Preferential Associations and Signatures of Phylosymbiosis

Microbial Ecology, Journal Year: 2023, Volume and Issue: 86(3), P. 2032 - 2046

Published: March 31, 2023

Ostreobium, the major algal symbiont of coral skeleton, remains understudied despite extensive research on holobiont. The enclosed nature skeleton might reduce dispersal and exposure residing bacteria to outside environment, allowing stronger associations with algae. Here, we describe bacterial communities associated cultured strains 5 Ostreobium clades using 16S rRNA sequencing. We shed light their likely physical by comparative analysis three datasets generated capture (1) all algae bacteria, (2) enriched tightly attached potential intracellular (3) in spent media. Our data showed that while some may be loosely attached, tend or potentially intracellular. Although colonised diverse preferentially 34 taxa revealing a core microbiome. These include known nitrogen cyclers, polysaccharide degraders, sulphate reducers, antimicrobial compound producers, methylotrophs, vitamin B12 producers. By analysing co-occurrence networks from Porites lutea Paragoniastrea australensis samples, show Ostreobium-bacterial present cultures are also occur natural environment. Finally, our significant congruence between phylogeny community composition its microbiome, largely due phylosymbiotic signal originating taxa. This study offers insight into microbiome reveals preferential warrant further testing functional evolutionary perspectives.

Language: Английский

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