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

Nature Reviews Microbiology volume 12, pages 686–698 (2014)Cite this article

Subjects

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 CO2 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.

Abstract

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.

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Figure 1: Bacterial transformation of phytoplankton-derived organic matter.
Figure 2: A representative bloom in the southern Pacific Ocean.
Figure 3: Changes in the abundance of roseobacter and flavobacteria phylotypes during a diatom-dominated bloom.
Figure 4: Physiological features of roseobacters that facilitate associations with phytoplankton.
Figure 5: Physiological features of flavobacteria that facilitate associations with phytoplankton.

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Acknowledgements

A.B. acknowledges support from the US National Science Foundation Division of Ocean Sciences (OCE-0550485 and OCE-1061352). J.M.G. was supported by the CONSOLIDER-INGENIO2010 Program (CSD2008-00077) and MarineGems (CTM2010-20361) from the Spanish Ministry of Science and Innovation.

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Authors and Affiliations

  1. Department of Microbiology, University of Tennessee, Knoxville, 37996-0845, Tennessee, USA

    Alison Buchan & Gary R. LeCleir

  2. School of Civil and Environmental Engineering, Georgia Institute of Technology, Atlanta, 30332, Georgia, USA

    Christopher A. Gulvik

  3. Department of Microbiology, University of La Laguna, La Laguna, ES-38200, Spain

    José M. González

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  1. Alison Buchan
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  2. Gary R. LeCleir
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  4. José M. González
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Correspondence to Alison Buchan.

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Glossary

Autotrophs

Organisms that convert inorganic carbon, such as CO2, into organic compounds.

Biological pump

The export of phytosynthetically derived carbon via the sinking of particles from the illuminated surface ocean to the deep ocean. Approximately 0.1% of the carbon that is fixed in the ocean is buried in marine sediments via this process.

Heterotrophic

A term used to describe an organism that uses organic carbon compounds, such as dissolved organic matter and particulate organic matter, to satisfy its carbon requirement but that cannot fix carbon.

Copiotrophic

A term used to describe an organism that thrives in, and is well adapted to, high-nutrient conditions, unlike oligotrophic organisms, which are adapted to growth in low-nutrient conditions.

Microbial loop

The microbial assimilation of dissolved organic matter into biomass and its transfer to higher trophic levels as a result of grazing by zooplankton.

Microbial carbon pump

A process by which a major reservoir of dissolved organic carbon is sequestered in the ocean by a series of heterotrophic microbial transformations of organic matter, which renders it increasingly resistant to biological degradation.

Dissolved organic matter

(DOM). The pool of organic matter that is operationally defined as that which passes through a filter with pores of 0.22–0.45 μm in diameter. DOM can be further classified on the basis of bioavailability.

Particulate organic matter

(POM). The pool of organic matter that is operationally defined as that which is retained on a filter with pores of 0.22–0.45 μm in diameter.

Cloud condensation nuclei

Aerosols (that is, liquid droplets or solid particles) suspended in the air that lead to the condensation of water vapour to form clouds.

Solar backscattered radiation

Solar radiation from the sun that is reflected back towards space by the atmosphere, clouds and the surface of the Earth.

Bacterioplankton

Free-living, planktonic bacteria and archaea that reside in an aquatic system.

Linnaean classification system

The taxonomic nomenclature that was developed by Carl Linnaeus, in which distinct hierarchical groups, such as phylum, class, order, family, genus and species are defined.

Remineralization

The transformation of organic matter to an inorganic form. This term is most often used to describe the conversion of organic carbon to CO2, which is a central component of the carbon cycle.

Euphotic zone

The layer of the water column that receives sufficient light to support photosynthesis. This zone is usually the upper 200 metres, but the lower boundary varies as the concentration of living and non-living particles change the turbidity of the water.

Benthic zone

The region of the water column that extends from immediately above the sediment surface to immediately below the sediment surface. Sinking material, such as marine snow, accumulates in this zone.

Pelagic zone

The upper region of the water column that is distant from land and from the seafloor. Water turbidity and light intensity do not shift the demarcation of the pelagic zone.

Diatomaceous earth

The remaining particulate matter from dead and decayed diatoms, which are heavily enriched in silica frustules.

Phylotypes

Sequences or groups of sequences that share a certain level of homology, which enables evolutionary relatedness to be inferred.

Ecological r-strategist model

Model organisms with relatively large genomes that encode diverse metabolic capabilities, which enable them to rapidly respond to increases in carbon and nutrients.

Phytodetrital material

Non-living organic matter that is derived from phytoplankton.

Auxins

A class of hormones that stimulate growth and regulate the behaviour of phototrophs.

Holdfasts

Adhesive structures that facilitate the attachment of a cell to a surface.

Aerobic anoxygenic phototrophy

A photoheterotrophic strategy in which bacteriochlorophyll a reaction centres are excited by the absorption of light and pass electrons through a series of carrier proteins that pump protons out of the cell, which contributes to the electrochemical gradient of the cell.

Photoheterotrophic

A term used to describe a heterotroph that uses light (that is, photons) to fuel energy-requiring metabolic processes.

Fosmid libraries

Libraries of cloning vectors derived from the bacterial F plasmid that stably maintain large fragments of DNA and are often used for sequencing or phenotypic screening.

Rhodopsins

Transmembrane proteins that function as light-driven ion pumps; they are present in all three domains of life.

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Buchan, A., LeCleir, G., Gulvik, C. et al. Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Microbiol 12, 686–698 (2014). https://doi.org/10.1038/nrmicro3326

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