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.

Swimming in the sea: chemotaxis by marine bacteria

“…The potential capacity of bacteria to use chemotaxis to take advantage of this microenvironment is notable given that marine heterotrophic bacteria obtain a large fraction of their carbon demand directly from phytoplankton, consuming up to 50% of phytoplankton-fixed carbon 21 . Recent studies using microfluidic experiments 22 and direct microscopic observations of chemotactic bacteria aggregating around phytoplankton cells 16 support predictions that bacterial chemotaxis will enhance bacterial uptake of phytoplankton derived carbon, as well as potentially underpinning the establishment and maintenance of important phytoplankton-bacteria relationships in the ocean 20 .…”

“…This behaviour is also involved in pathogenicity and disease outbreaks among a wide range of marine species 32,33 , both in natural habitats 27 and in aquaculture settings 34 , sometimes with dire ecological and economic consequences. In the pelagic environment, chemotaxis plays an often pivotal role in all major biogeochemical cycles, by affecting the rates and directions of key chemical transformations 1,9,20 . For example, chemotaxis-mediated particle colonisation influences controls the amount of carbon that either sinks to the deep sea or is respired in the upper ocean, ultimately influencing global carbon budgets …”

“…This led to the hypothesis that marine bacteria will use chemotaxis to colonise the 'phycosphere' -the region immediately surrounding a phytoplankton cell that is enriched in exuded organic substrates 20 ( Figure 2). The potential capacity of bacteria to use chemotaxis to take advantage of this microenvironment is notable given that marine heterotrophic bacteria obtain a large fraction of their carbon demand directly from phytoplankton, consuming up to 50% of phytoplankton-fixed carbon 21 .…”

Iron and Harmful Algae Blooms: Potential Algal-Bacterial Mutualism Between Lingulodinium polyedrum and Marinobacter algicola

“…While numerous studies concentrate on the causes of HABs, few have considered that bacterial species coexisting with microalgae could contribute to their development. However since Bell and Mitchell reported that specific bacterial communities occur and microbial activity was altered in the so-called phycosphere (Bell and Mitchell, 1972;Bell and Lang, 1974), more and more studies suggest that such algalbacterial interactions are very specific and important (Azam and Malfatti, 2007;Amin et al, 2015;Bertrand et al, 2015;Ramanan et al, 2016;Seymour et al, 2017). A plausible hypothesis suggests that the mutualistic association of some phytoplankton and bacteria is based on nutrient exchange.…”

Identification of Bacterial Genes Expressed During Diatom-Bacteria Interactions Using an in Vivo Expression Technology Approach

“…Recently, Behringer et al (2018) demonstrated that bacterial communities on diatom surfaces displayed strong conservation across diatom strains. Seymour et al (2017) elegantly summarized the main corresponding mechanisms and processes, which show an impressive array of diversity and complexity.…”