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Zooming in on the Phycosphere: the Ecological Interface for Phytoplankton–Bacteria Relationships Justin R

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Zooming in on the Phycosphere: the Ecological Interface for Phytoplankton–Bacteria Relationships Justin R REVIEW ARTICLE PUBLISHED: 30 MAY 2017 | VOLUME: 2 | ARTICLE NUMBER: 17065 Zooming in on the phycosphere: the ecological interface for phytoplankton–bacteria relationships Justin R. Seymour1*, Shady A. Amin2,3, Jean-Baptiste Raina1 and Roman Stocker4 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 spa- tiotemporal 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 col- onization 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. ithin the context of ecosystem function (Box 1), the eco- relationships from cooperative to competitive13. At the simplest level, logical relationships between phytoplankton and bacteria the relationship between these organisms is based on resource pro- Warguably represent the most important inter-organism vision and can be either reciprocal or exploitative in nature2 (Fig. 1). association in aquatic environments. Te interactions between Aquatic heterotrophic bacteria obtain a large, albeit variable, frac- these two groups strongly infuence carbon and nutrient cycling, tion of their carbon demand directly from phytoplankton14, with regulate the productivity and stability of aquatic food webs, and up to 50% of the carbon that is fxed by phytoplankton ultimately afect ocean–atmosphere fuxes of climatically relevant chemicals1–3. consumed by bacteria15. Bacterial consumption of phytoplankton- Indeed, the shared evolutionary history of these organisms4 has derived organic material primarily involves the assimilation of the undoubtedly played an important role in shaping aquatic ecosystem large quantities of typically highly labile, dissolved organic carbon function and global biogeochemistry. (DOC) (Box 1) released by phytoplankton cells into the surround- Within aquatic ecosystems, phytoplankton are the dominant pri- ing water column16, but also includes consumption of more complex mary producers and the base of the food web. Consistent with their algal products (for example, mucilage and polysaccharides)17,18 and common functional roles, we here consider the phytoplankton to senescent or dead phytoplankton biomass19. include both microalgae (for example, diatoms and dinofagellates) From the perspective of a phytoplankton cell, bacteria can be pro- and oxygenic phototrophic cyanobacteria (such as Prochlorococcus, viders of limiting macronutrients via remineralization20,21 (Box 1), Synechococcus and Anabaena). Together, these organisms are but also competitors for inorganic nutrients22. When the allochtho- responsible for almost 50% of global photosynthesis and are conse- nous (Box 1) supply of nutrients is low, phytoplankton growth is quently important regulators of global carbon and oxygen fuxes5,6. predicted to particularly beneft from bacterial delivery of regen- Te abundance and metabolism of aquatic heterotrophic bacte- erated nitrogen and phosphorus2. Furthermore, evidence for the ria (Box 1), which represent about a quarter of all biomass in the development of specifc phytoplankton–bacteria interactions based 7 12,23 euphotic zone of aquatic habitats and the engine room for Earth’s on bacterial synthesis of vitamins (for example, vitamin B12) and major biogeochemical cycles8, are intrinsically linked to phyto- enhancement of micronutrient (for example, Fe) bioavailability24 plankton production and biomass9,10. Indeed, while phytoplankton has begun to highlight the complex nature of the ecological links and bacteria are both fundamental biotic features of aquatic habitats between these groups of aquatic microorganisms. in their own right, the strong ecological coupling between these two Evidence for intimate and selective associations between groups demands that the nature and consequences of their synergis- phytoplankton and bacteria is further provided by the consist- tic infuences are explicitly considered. ent detection of particular bacterial species from phytoplankton Phytoplankton–bacteria interactions are multifarious and ofen cultures and algal blooms11,24–28, which has led to the proposition highly sophisticated11,12, and can span the spectrum of ecological that ‘archetypal phytoplankton-associated bacterial taxa’ exist29. 1Climate Change Cluster (C3), University of Technology Sydney, New South Wales 2007, Australia. 2Department of Biology, New York University Abu Dhabi, PO Box 129188, Abu Dhabi, United Arab Emirates. 3Department of Chemistry, New York University Abu Dhabi, PO Box 129188, Abu Dhabi, United Arab Emirates. 4Institute of Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, Stefano-Franscini-Platz 5, 8093 Zurich, Switzerland. *e-mail: [email protected] NATURE MICROBIOLOGY 2, 17065 (2017) | DOI: 10.1038/nmicrobiol.2017.65 | www.nature.com/naturemicrobiology 1 ǟ ƐƎƏƗ !,(++- 4 +(2'#12 (,(3#"Ʀ /13 .$ /1(-%#1 341#ƥ ++ 1(%'32 1#2#15#"ƥ ɥ ɥ ɥ ɥ ɥ ɥ ɥ ɥ ɥ ɥ ɥ REVIEW ARTICLE NATURE MICROBIOLOGY Box 1 | Glossary. Ecosystem function. Te collective infuence of an ecosystem’s Phycosphere. Te region immediately surrounding a phytoplank- biodiversity, physical properties and chemical features on the ton cell that is enriched in organic molecules exuded by the cell trophic and biogeochemical links, transfers and fuxes within the into the surrounding water. system, including the subsequent impacts of these processes on Rhizosphere. Te zone immediately surrounding the roots the wider biosphere. of a plant that is enriched in molecules secreted from the root Heterotrophic. An organism that must acquire organic carbon into the soil, providing a key interface for the ecological rela- from its environment for sustaining growth and generating energy. tionships and chemical exchanges between plants and soil Dissolved organic carbon. Te large reservoir of organic mate- microorganisms. rial found in aquatic ecosystems that is operationally defned as Phytostimulator. An organism or chemical that promotes plant ‘dissolved’ by its ability to pass through a 0.22 μm flter (although growth. sometimes this cut-of is defned at 0.45 μm). Bioavailability. Te quality of a molecule or material that renders Remineralization. Te transformation of organic material into it metabolically utilizable to a living organism. simple inorganic components. Diazotrophic. Te capacity of some prokaryotes to fx atmos- Allochthonous. A material that is imported into an ecosystem pheric dinitrogen gas into more biologically available forms of from an external source. nitrogen (such as ammonium). Tese observations are corroborated by global surveys that show phycosphere exists”. Here, we consider not only the existence of that phytoplankton-associated bacterial communities are ofen the phycosphere, but also its signifcance within aquatic habitats, restricted to only a handful of groups30, including specifc members by frst exploring the physical and chemical processes that control of the Roseobacter clade (Rhodobacteraceae), Flavobacteraceae and its formation and persistence within the environment, and then Alteromonadaceae13,18,25,26,28,30. Tese apparently universal patterns assessing its ecological importance by examining how it facilitates imply that the lifestyles of some bacteria within these groups are interactions between phytoplankton and bacteria. profoundly defned by their interaction with phytoplankton, and likewise there is evidence that phytoplankton can either beneft12 or The phycosphere as a fundamental ecological interface sufer28 from the presence of these key bacterial groups. Before examining the ecological relevance of the phycosphere, it is In line with evidence for species-specifc associations29,31 and instructive to consider the inherent physical and chemical features the ofen reciprocal nature of the metabolic exchanges between of this unique aquatic microenvironment and relate these character- bacteria and phytoplankton11,12,24, there is an emerging view that istics to other analogous systems. phytoplankton–bacteria interactions
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