Abstract

SummaryMarine phototroph and heterotroph interactions are vital in maintaining the nutrient balance in the oceans as essential nutrients need to be rapidly cycled before sinking to aphotic layers. The aim of this study was to highlight the molecular mechanisms that drive these interactions. For this, we generated a detailed exoproteomic time‐course analysis of a 100‐day co‐culture between the model marine picocyanobacterium Synechococcus sp. WH7803 and the Roseobacter strain Ruegeria pomeroyi DSS‐3, both in nutrient‐enriched and natural oligotrophic seawater. The proteomic data showed a transition between the initial growth phase and stable‐state phase that, in the case of the heterotroph, was caused by a switch in motility attributed to organic matter availability. The phototroph adapted to seawater oligotrophy by reducing its selective leakiness, increasing the acquisition of essential nutrients and secreting conserved proteins of unknown function. We also report a surprisingly high abundance of extracellular superoxide dismutase produced by Synechococcus and a dynamic secretion of potential hydrolytic enzyme candidates used by the heterotroph to cleave organic groups and hydrolase polymeric organic matter produced by the cyanobacterium. The time course dataset we present here will become a reference for understanding the molecular processes underpinning marine phototroph‐heterotroph interactions.

Highlights

  • The ocean is the Earth’s largest biome covering 70% of the world’s surface

  • This is a process whereby CO2 in the upper ocean is fixed by photosynthetic primary producers to form organic matter that is transported to the deeper ocean by sedimenting particulate organic matter (POM) and the drawdown of dissolved organic matter (DOM) through mixing and dwelling (Jiao et al, 2010)

  • WH7803 reaches high cell densities in artificial seawater (ASW) (> 109 cells ml21) and growth is limited by light, in natural SW the cyanobacterium is limited by the availability of inorganic nutrients and cell densities reached 105 cells ml21, numbers that are similar to those observed in natural marine ecosystems (Parsons et al, 2012)

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Summary

Introduction

The ocean is the Earth’s largest biome covering 70% of the world’s surface. Marine systems play a major role in global climate regulation, due to their ability to store and transport heat, and because of the constant atmosphere—ocean exchange of CO2. Phytoplankton are at the base of the marine food chain feeding the ecosystem with DOM and POM that is released via cell lysis (e.g., cell death, inefficient grazing and viral lysis) or other cellular processes (e.g., outer membrane vesicles, active efflux processes or permeable membrane leakage) (Biller et al, 2014; Christie-Oleza et al, 2015a,; Grossowicz et al, 2017) Most of this organic matter will be used by the heterotrophic bacterioplankton as their main source of carbon and energy, returning inorganic nutrients to the phototrophic community (Christie-Oleza et al, 2017).

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