Abstract

There is a growing appreciation within animal and plant physiology that the reactive oxygen species (ROS) superoxide is not only detrimental but also essential for life. Yet, despite widespread production of extracellular superoxide by healthy bacteria and phytoplankton, this molecule remains associated with stress and death. Here, we quantify extracellular superoxide production by seven ecologically diverse bacteria within the Roseobacter clade and specifically target the link between extracellular superoxide and physiology for two species. We reveal for all species a strong inverse relationship between cell-normalized superoxide production rates and cell number. For exponentially growing cells of Ruegeria pomeroyi DSS-3 and Roseobacter sp. strain AzwK-3b, we show that superoxide levels are regulated in response to cell density through rapid modulation of gross production and not decay. Over a life cycle of batch cultures, extracellular superoxide levels are tightly regulated through a balance of both production and decay processes allowing for nearly constant levels of superoxide during active growth and minimal levels upon entering stationary phase. Further, removal of superoxide through the addition of exogenous superoxide dismutase during growth leads to significant growth inhibition. Overall, these results point to tight regulation of extracellular superoxide in representative members of the Roseobacter clade, consistent with a role for superoxide in growth regulation as widely acknowledged in fungal, animal, and plant physiology.IMPORTANCE Formation of reactive oxygen species (ROS) through partial reduction of molecular oxygen is widely associated with stress within microbial and marine systems. Nevertheless, widespread observations of the production of the ROS superoxide by healthy and actively growing marine bacteria and phytoplankton call into question the role of superoxide in the health and physiology of marine microbes. Here, we show that superoxide is produced by several marine bacteria within the widespread and abundant Roseobacter clade. Superoxide levels outside the cell are controlled via a tightly regulated balance of production and decay processes in response to cell density and life stage in batch culture. Removal of extracellular superoxide leads to substantial growth inhibition. These findings point to an essential role for superoxide in the health and growth of this ubiquitous group of microbes, and likely beyond.

Highlights

  • IMPORTANCE Formation of reactive oxygen species (ROS) through partial reduction of molecular oxygen is widely associated with stress within microbial and marine systems

  • Despite its perceived role as an indicator of stress, extracellular superoxide production has been observed in healthy, actively growing cells encompassing a wide taxonomy of common marine organisms, including the diazotroph Trichodesmium, cyanobacterium Synechococcus, diatoms Thalassiosira spp., and various marine algae and heterotrophic bacteria [2, 4, 6, 8, 18,19,20,21]

  • High levels of extracellular superoxide have been observed for representative members of the Roseobacter clade of heterotrophic alphaproteobacteria grown under ideal conditions in culture [2, 5]

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Summary

Introduction

IMPORTANCE Formation of reactive oxygen species (ROS) through partial reduction of molecular oxygen is widely associated with stress within microbial and marine systems. Despite the clear difference in superoxide levels for a given volume of culture (representative of a given volume within the flask), superoxide concentrations and cell-normalized production rates were not significantly different across dilution conditions when equivalent numbers of cells were added to the filter (Fig. 5).

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