Dataset Information

Microbial gardening in the ocean's twilight zone: detritivorous metazoans benefit from fragmenting, rather than ingesting, sinking detritus: fragmentation of refractory detritus by zooplankton beneath the euphotic zone stimulates the harvestable production of labile and nutritious microbial biomass.

ABSTRACT: Sinking organic particles transfer ?10?gigatonnes of carbon into the deep ocean each year, keeping the atmospheric CO2 concentration significantly lower than would otherwise be the case. The exact size of this effect is strongly influenced by biological activity in the ocean's twilight zone (?50-1,000?m beneath the surface). Recent work suggests that the resident zooplankton fragment, rather than ingest, the majority of encountered organic particles, thereby stimulating bacterial proliferation and the deep-ocean microbial food web. Here we speculate that this apparently counterintuitive behaviour is an example of 'microbial gardening', a strategy that exploits the enzymatic and biosynthetic capabilities of microorganisms to facilitate the 'gardener's' access to a suite of otherwise unavailable compounds that are essential for metazoan life. We demonstrate the potential gains that zooplankton stand to make from microbial gardening using a simple steady state model, and we suggest avenues for future research.

SUBMITTER: Mayor DJ

PROVIDER: S-EPMC4278546 | biostudies-literature | 2014 Dec

REPOSITORIES: biostudies-literature

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Microbial gardening in the ocean's twilight zone: detritivorous metazoans benefit from fragmenting, rather than ingesting, sinking detritus: fragmentation of refractory detritus by zooplankton beneath the euphotic zone stimulates the harvestable production of labile and nutritious microbial biomass.

Mayor Daniel J DJ Sanders Richard R Giering Sarah L C SL Anderson Thomas R TR

BioEssays : news and reviews in molecular, cellular and developmental biology 20140912 12

Sinking organic particles transfer ∼10 gigatonnes of carbon into the deep ocean each year, keeping the atmospheric CO2 concentration significantly lower than would otherwise be the case. The exact size of this effect is strongly influenced by biological activity in the ocean's twilight zone (∼50-1,000 m beneath the surface). Recent work suggests that the resident zooplankton fragment, rather than ingest, the majority of encountered organic particles, thereby stimulating bacterial proliferation a ...[more]

PMID: 25220362

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Project description:The twilight zone (from the base of the euphotic zone to the depth of 1,000 m) is the major area of particulate organic carbon (POC) remineralization in the ocean, and heterotrophic microbes contribute to more than 70% of the estimated remineralization. However, little is known about the microbial community and metabolic activity directly associated with POC remineralization in this chronically understudied realm. Here, we characterized the microbial community proteomes of POC samples collected from the twilight zone of three contrasting sites in the Northwest Pacific Ocean using a metaproteomic approach. The particle-attached bacteria from Alteromonadales, Rhodobacterales, and Enterobacterales were the primary POC remineralizers. Hydrolytic enzymes, including proteases and hydrolases, that degrade proteinaceous components and polysaccharides, the main constituents of POC, were abundant and taxonomically associated with these bacterial groups. Furthermore, identification of diverse species-specific transporters and metabolic enzymes implied niche specialization for nutrient acquisition among these bacterial groups. Temperature was the main environmental factor driving the active bacterial groups and metabolic processes, and Enterobacterales replaced Alteromonadales as the predominant group under low temperature. This study provides insight into the key bacteria and metabolic processes involved in POC remineralization, and niche complementarity and species substitution among bacterial groups are critical for efficient POC remineralization in the twilight zone. IMPORTANCE The ocean's twilight zone is a critical zone where more than 70% of the sinking particulate organic carbon (POC) is remineralized. Therefore, the twilight zone determines the size of biological carbon storage in the ocean and regulates the global climate. Prokaryotes are major players that govern remineralization of POC in this region. However, knowledge of microbial community structure and metabolic activity is still lacking. This study unveiled microbial communities and metabolic activities of POC samples collected from the twilight zone of three contrasting environments in the Northwest Pacific Ocean using a metaproteomic approach. Alteromonadales, Rhodobacterales, and Enterobacterales were the major remineralizers of POC. They excreted diverse species-specific hydrolytic enzymes to split POC into solubilized POC or dissolved organic carbon. Temperature played a crucial role in regulating the community composition and metabolism. Furthermore, niche complementarity or species substitution among bacterial groups guaranteed the efficient remineralization of POC in the twilight zone.

Dataset Information

Microbial gardening in the ocean's twilight zone: detritivorous metazoans benefit from fragmenting, rather than ingesting, sinking detritus: fragmentation of refractory detritus by zooplankton beneath the euphotic zone stimulates the harvestable production of labile and nutritious microbial biomass.

Publications

Microbial gardening in the ocean's twilight zone: detritivorous metazoans benefit from fragmenting, rather than ingesting, sinking detritus: fragmentation of refractory detritus by zooplankton beneath the euphotic zone stimulates the harvestable production of labile and nutritious microbial biomass.

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