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Zooming in on the phycosphere: the ecological interface for phytoplankton–bacteria relationships

Abstract

By controlling nutrient cycling and biomass production at the base of the food web, interactions between phytoplankton and bacteria represent a fundamental ecological relationship in aquatic environments. Although typically studied over large spatiotemporal scales, emerging evidence indicates that this relationship is often governed by microscale interactions played out within the region immediately surrounding individual phytoplankton cells. This microenvironment, known as the phycosphere, is the planktonic analogue of the rhizosphere in plants. The exchange of metabolites and infochemicals at this interface governs phytoplankton–bacteria relationships, which span mutualism, commensalism, antagonism, parasitism and competition. The importance of the phycosphere has been postulated for four decades, yet only recently have new technological and conceptual frameworks made it possible to start teasing apart the complex nature of this unique microbial habitat. It has subsequently become apparent that the chemical exchanges and ecological interactions between phytoplankton and bacteria are far more sophisticated than previously thought and often require close proximity of the two partners, which is facilitated by bacterial colonization of the phycosphere. It is also becoming increasingly clear that while interactions taking place within the phycosphere occur at the scale of individual microorganisms, they exert an ecosystem-scale influence on fundamental processes including nutrient provision and regeneration, primary production, toxin biosynthesis and biogeochemical cycling. Here we review the fundamental physical, chemical and ecological features of the phycosphere, with the goal of delivering a fresh perspective on the nature and importance of phytoplankton–bacteria interactions in aquatic ecosystems.

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Figure 1: Phytoplankton–bacteria interactions and exchanges.
Figure 2: The rhizosphere and the phycosphere are analogous microenvironments.
Figure 3: The effect of mild to moderate turbulence on the phycosphere.
Figure 4: Bacteria may encounter and, in some cases, retain contact with the phycosphere through several means.
Figure 5: Depiction of mutualistic (left) and algicidal (right) phytoplankton–bacteria interactions expected to occur in the phycosphere.
Figure 6: Potential large-scale implications of processes taking place within the phycosphere.

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Acknowledgements

We thank V. Fernandez for assistance with the calculations performed to characterize physical features of the phycosphere and G. Gorick for assisting with the design of the figures. This research was funded in part by the Gordon and Betty Moore Foundation Marine Microbiology Initiative, through grant GBMF3801 to J.R.S. and R.S. and an Investigator Award (GBMF3783) to R.S., and an Australian Research Council grant (DP140101045) to J.R.S. J.R.S. and J.-B.R. were supported by Australian Research Council fellowships FT130100218 and DE160100636 respectively.

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J.R.S., S.A.A., J.-B.R. and R.S. conceived the study, researched the literature and wrote the manuscript.

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Correspondence to Justin R. Seymour.

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Seymour, J., Amin, S., Raina, JB. et al. Zooming in on the phycosphere: the ecological interface for phytoplankton–bacteria relationships. Nat Microbiol 2, 17065 (2017). https://doi.org/10.1038/nmicrobiol.2017.65

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