Journal Article

Master recyclers: features and functions of bacteria associated with phytoplankton blooms

LeCleir, Gary R., Buchan, Alison, Gulvik, Christopher A., González, José M.

2014

Overview

Key Points Phytoplankton are the most abundant primary producers in the oceans, and phytoplankton blooms are recognizable signs of the annual productivity cycle in aquatic systems. Phytoplankton blooms contain dense and diverse heterotrophic bacterial populations that determine the fate of much of the carbon that is fixed by these primary producers. This is achieved by the transformation of phytoplankton-derived organic matter, which returns carbon to the atmosphere as CO 2 and converts carbon to bacterial biomass, which enters the marine food web or renders it resistant to microbial degradation, such that it contributes to a vast pool of recalcitrant carbon in the ocean. Although blooms vary in terms of phytoplankton composition and environmental conditions, a limited number of bacterial taxa dominate bloom-associated microbial communities. The most frequently observed bacteria belong to the Flavobacteriia and Proteobacteria. Cultivated representatives of both flavobacteria and roseobacters are currently the main models that are used to study phytoplankton–bacteria interactions. These two lineages show substantial metabolic versatility, which seems to fuel these interactions. Culture-based studies of roseobacters suggest that they form more intimate associations with specific phytoplankton than flavobacteria. Specific physiological processes that have been identified in cultured representatives and are supported by metagenomic data from natural populations have been proposed to facilitate these interactions. These include the production of secondary metabolites, catabolism of various phytoplankton-derived low molecular weight compounds and cell surface structures that facilitate cellular adhesion. Genomic, metatranscriptomic and metaproteomic data suggest that flavobacteria are particularly well equipped to use the high molecular weight components of phytoplankton-derived material. Other flavobacterial physiologies, including cell adhesion and motility, may be important in facilitating interactions between flavobacteria and phytoplankton. Marine phytoplankton blooms are annual spring events that are accompanied by a surge in heterotrophic bacteria, primarily roseobacters, flavobacteria and members of the Gammaproteobacteria, which recycle most of the carbon that is fixed by the primary producers. In this Review, Buchan et al . describe the emerging physiological features and functions of these bacterial communities and their interactions with phytoplankton. Marine phytoplankton blooms are annual spring events that sustain active and diverse bloom-associated bacterial populations. Blooms vary considerably in terms of eukaryotic species composition and environmental conditions, but a limited number of heterotrophic bacterial lineages — primarily members of the Flavobacteriia, Alphaproteobacteria and Gammaproteobacteria — dominate these communities. In this Review, we discuss the central role that these bacteria have in transforming phytoplankton-derived organic matter and thus in biogeochemical nutrient cycling. On the basis of selected field and laboratory-based studies of flavobacteria and roseobacters, distinct metabolic strategies are emerging for these archetypal phytoplankton-associated taxa, which provide insights into the underlying mechanisms that dictate their behaviours during blooms.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 631/326/171 / 631/326/2565/855 / 631/326/41/1969 / 631/326/41/2535 / Alphaproteobacteria - growth & development / Alphaproteobacteria - metabolism / Aquatic Organisms / Bacteria / Biogeochemical cycles / Biogeochemistry / Biomass / Carbon / Carbon cycle / Environment / Environmental aspects / Environmental conditions / Eutrophication / Flavobacteria / Flavobacteriaceae - growth & development / Flavobacteriaceae - metabolism / Food chains / Gammaproteobacteria - growth & development / Gammaproteobacteria - metabolism / Growth / Infectious Diseases / Life Sciences / Medical Microbiology / Microbial colonies / Microbiology / Nitrogen / Nutrient cycles / Nutrients / Organic Chemicals - metabolism / Organic matter / Organisms / Parasitology / Phytoplankton / Phytoplankton - growth & development / Phytoplankton - metabolism / Phytoplankton - microbiology / Plankton / Respiration / review-article / Roseobacter / Species composition / Taxa / Virology / Water bloom