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

Journal name:
Nature Reviews Microbiology
Volume:
12,
Pages:
686–698
Year published:
DOI:
doi:10.1038/nrmicro3326
Published online

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.

At a glance

Figures

  1. Bacterial transformation of phytoplankton-derived organic matter.
    Figure 1: Bacterial transformation of phytoplankton-derived organic matter.

    The marine carbon cycle includes a number of processes, several of which are mediated by microorganisms. Key processes of the marine carbon cycle include the conversion of inorganic carbon (such as CO2) to organic carbon by photosynthetic phytoplankton species (step 1); the release of both dissolved organic matter (DOM; which includes dissolved organic carbon (DOC), dissolved organic nitrogen (DON) and dissolved organic phosphorous (DOP)) and particulate organic matter (POM; which includes particulate organic carbon (POC), particulate organic nitrogen (PON) and particulate organic phosphorous (POP)) from phytoplankton (step 2); the consumption of phytoplankton biomass by zooplankton grazers (step 3) and the mineralization (that is the release of CO2 via respiration during the catabolism of organic matter) and recycling of organic matter by diverse heterotrophic bacteria, including, but not limited to, flavobacteria and roseobacters (which is known as the microbial loop; step 4). A fraction of the heterotrophic bacteria is consumed by zooplankton, and the carbon is further transferred up the food web. Heterotrophic bacteria also contribute to the remineralization of organic nutrients, including DON and DOP, to inorganic forms, which are then available for use by phytoplankton. The microbial carbon pump (step 5) refers to the transformation of organic carbon into recalcitrant DOC that resists further degradation and is sequestered in the ocean for thousands of years. The biological pump (step 6) refers to the export of phytoplankton-derived POM from the surface oceans to deeper depths via sinking. Finally, the viral shunt (step 7) describes the contributions of viral-mediated cell lysis to the release of dissolved and particulate matter from both the phytoplankton and bacterial pools.

  2. A representative bloom in the southern Pacific Ocean.
    Figure 2: A representative bloom in the southern Pacific Ocean.

    Spring phytoplankton blooms are a natural part of the seasonal productivity cycle of many marine systems. These blooms are transient events that typically last for several weeks and are large enough to be visible from space. a | A satellite image of the eastern coast of New Zealand before a bloom on 11 October 2009 is shown. b | The satellite image shows the same region during a diatom-dominated bloom on 29 October 2009. Such blooms are annual occurrences in this region and the phytoplankton composition of these blooms have been characterized26. c | The graph shows a typical succession of phytoplankton groups during the course of a spring phytoplankton bloom in this region of the ocean, which often lasts for many weeks (data taken from Ref. 26). Changes in the relative abundance of heterotrophic bacteria and nanoflagellate grazers are also indicated to show the increase in bacterial abundance in response to increases in phytoplankton, in addition to the increase in grazers in response to increases in their prey populations (such as bacteria and phytoplankton). The satellite images were captured by the Moderate Resolution Imaging Spectroradiometer (MODIS) on NASA Aqua satellite during the 2009 austral spring and were generated by R. Simmon and J. Allen, Ocean Colour Team, NASA, USA.

  3. Changes in the abundance of roseobacter and flavobacteria phylotypes during a diatom-dominated bloom.
    Figure 3: Changes in the abundance of roseobacter and flavobacteria phylotypes during a diatom-dominated bloom.

    A high-resolution analysis of the bacterial community during a natural spring diatom-dominated phytoplankton bloom in the North Sea shows the succession of specific roseobacter and flavobacteria phylotypes. a | Chlorophyll a measurements are a proxy for phytoplankton abundance during the course of the 90 day survey. Despite the coarse temporal resolution, it is evident that the increase in bacterial abundance coincides with the decline in phytoplankton (following an initial surge), which is probably due to the increased availability of phytoplankton organic matter fuelling bacterial growth. b | Compared with all other bacteria, the relative abundance of roseobacters and flavobacteria increased during the bloom. The values above each stacked column represent the percent abundance of each group member relative to total bacteria, as determined by 16S ribosomal RNA gene sequence analysis. The relative abundances of roseobacters and flavobacteria, as well as specific phylotypes (as indicated in the key), are dynamic throughout the bloom. These complex dynamics are probably the result of tight coupling between these heterotrophic bacteria and changing local environmental conditions, which are expected to be primarily mediated by alterations in the availability of phytoplankton-derived organic matter and possibly inorganic nutrient levels. Data taken from Ref. 17.

  4. Physiological features of roseobacters that facilitate associations with phytoplankton.
    Figure 4: Physiological features of roseobacters that facilitate associations with phytoplankton.

    Roseobacters have many metabolic features that probably facilitate interactions with phytoplankton and phytodetrital material. The organic sulphur compound dimethylsulphoniopropionate (DMSP) is produced by phytoplankton and transformed via one of two pathways: cleavage to form dimethyl sulphide (DMS) and acrylate or demethylation to form methanethiol (MeSH). DMS is volatile and fluxes to the atmosphere, where it contributes to cloud formation, whereas the acrylate by-product can be used as a carbon source by the bacteria. MeSH is also a valuable carbon substrate, from which reduced sulphur is derived. Indeed, roseobacters use a wide range of low molecular weight, phytoplankton-derived compounds as sources of carbon, nitrogen and phosphorus (depicted as dissolved organic matter (DOM)). Chemotaxis towards several of these phytoplankton-derived compounds has been demonstrated and roseobacters encode several transport systems that are predicted to mediate the uptake of small molecules, including ATP-dependent transporters (such as ATP-binding cassette (ABC) transporters) and secondary transporters that may use electrochemical gradients to mediate membrane translocation, such as TRAP (tripartite ATP-independent periplasmic) and drug–metabolite (DMT) type systems. TRAP transporters are thought to import carboxylic acids, whereas DMT transporters are thought to export secondary metabolites, including phytoplankton growth-promoting compounds (such as auxins and vitamins) and antimicrobial compounds that may provide roseobacters with a competitive advantage when colonizing the surfaces of phytoplankton. Quorum sensing signalling molecules, typically N-acyl homoserine lactones (AHLs), are produced by many roseobacter strains and have been shown to regulate the production of antimicrobial compounds in a cell density-dependent manner. In addition to the oxidation of organic matter, many roseobacter genomes encode bacteriochlorophyll a-based light-driven proton pumps that contribute to membrane electrochemical gradients, which can be used to generate ATP via ATP synthases, facilitate transport or drive flagellar motors. Adhesive structures for attachment to surfaces are also commonly observed in roseobacter isolates. POM, particulate organic matter.

  5. Physiological features of flavobacteria that facilitate associations with phytoplankton.
    Figure 5: Physiological features of flavobacteria that facilitate associations with phytoplankton.

    Flavobacteria genomes encode several physiological processes that probably contribute to their interactions with phytoplankton and phytoplankton-derived organic matter. These include membrane-associated and extracellular hydrolytic enzymes, such as laminarinases and β-D-fucosidases, for the degradation of high molecular weight compounds that cannot pass through bacterial cell membranes. Flavobacteria have highly efficient, multiprotein extracellular systems that bind to large molecules, enzymatically digest them, and then shuttle the products through dedicated transport systems, such as TonB-dependent transport (TBDT) systems. Flavobacteria have additional transporters that are both ATP-dependent (ATP-binding cassette (ABC)-type) and ATP-independent (that is, secondary transporters) that facilitate the uptake of low molecular weight components of phytoplankton dissolved organic matter (DOM). Some strains have cell surface motility adhesins, such as SprB and RemA, which are necessary for gliding motility over surfaces. Other surface proteins, which are predicted to be adhesins owing to the presence of conserved, repetitive peptide motifs, may facilitate attachment to both living and dead surfaces, such as particulate organic matter (POM). Virulence factors, such as proteases, are encoded in some flavobacteria genomes and might have algicidal properties. Many flavobacteria genomes also encode rhodopsins that function as light-driven ion (H+, Cl, or Na+) pumps. Although their function during phytoplankton blooms has not been elucidated, H+ and Na+ gradients can be used to drive substrate translocation or ATP production via ATP synthases, whereas Cl pumps are probably involved in maintaining an appropriate intracellular ion balance.

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Affiliations

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

    • Alison Buchan &
    • Gary R. LeCleir
  2. School of Civil and Environmental Engineering, Georgia Institute of Technology, Atlanta, Georgia 30332, USA.

    • Christopher A. Gulvik
  3. Department of Microbiology, University of La Laguna, ES-38200 La Laguna, Spain.

    • José M. González

Competing interests statement

The authors declare no competing interests.

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Author details

  • Alison Buchan

    Alison Buchan received her Ph.D. in marine sciences from the University of Georgia, Athens, USA. She is currently Associate Professor of Microbiology at the University of Tennessee in Knoxville, Tennessee, USA, and her research interests are broadly in the area of marine microbial ecology, with particular emphasis on understanding the physiologies of Roseobacter spp. that contribute to their success in various marine niches.

  • Gary R. LeCleir

    Gary R. LeCleir received his Ph.D. in marine sciences from the University of Georgia, Athens, USA. He is currently a research associate in the Department of Microbiology at the University of Tennessee in Knoxville, Tennessee, USA, and his research interests include microbial community diversity and function in varied environments.

  • Christopher A. Gulvik

    Christopher A. Gulvik received his Ph.D. in microbiology from the University of Tennessee in Knoxville, Tennessee, in 2013 and is currently a postdoctoral associate in the Department of Civil and Environmental Engineering at Georgia Institute of Technology in Atlanta, Georgia, USA. He is interested in the enzymatic pathways that are used by bacteria to degrade aromatic compounds.

  • José M. González

    José M. González received his Ph.D. in microbiology from the University of Georgia, Athens, USA. He is now Associate Professor of Microbiology at the University of La Laguna, Spain. His research interests are focused on genomics and metagenomics for the study of microbial ecology.

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