Abstract
ABSTRACTBacteria and eukaryotes produce the reactive oxygen species superoxide both within and outside the cell. Although superoxide is typically associated with the detrimental and sometimes fatal effects of oxidative stress, it has also been shown to be involved in a range of essential biochemical processes, including cell signaling, growth, differentiation, and defense. Light‐independent extracellular superoxide production has been shown to be widespread among many marine heterotrophs and phytoplankton, but the extent to which this trait is relevant to marine microbial physiology and ecology throughout the global ocean is unknown. Here, we investigate the dark extracellular superoxide production of five groups of organisms that are geographically widespread and represent some of the most abundant organisms in the global ocean. These include Prochlorococcus, Synechococcus, Pelagibacter, Phaeocystis, and Geminigera. Cell‐normalized net extracellular superoxide production rates ranged seven orders of magnitude, from undetectable to 14,830 amol cell−1 h−1, with the cyanobacterium Prochlorococcus being the lowest producer and the cryptophyte Geminigera being the most prolific producer. Extracellular superoxide production exhibited a strong inverse relationship with cell number, pointing to a potential role in cell signaling. We demonstrate that rapid, cell‐number–dependent changes in the net superoxide production rate by Synechococcus and Pelagibacter arose primarily from changes in gross production of extracellular superoxide, not decay. These results expand the relevance of dark extracellular superoxide production to key marine microbes of the global ocean, suggesting that superoxide production in marine waters is regulated by a diverse suite of marine organisms in both dark and sunlit waters.
Highlights
IntroductionThe reasons and mechanisms of extracellular superoxide production within marine microbes have only been minimally explored and remain unclear, a wide diversity of photoautotrophic and heterotrophic microbes have been shown to produce superoxide outside their cells under both light and dark conditions in natural waters (Rose et al 2008b; Diaz et al 2013; Hansel et al 2016)
We examine the extracellular production by cyanobacteria Synechococcus and Prochlorococcus, the two most abundant photosynthesizing organisms in the global ocean
Extracellular superoxide by key marine microbes Extracellular superoxide production has long been established as a characteristic of fungi and higher plants, yet it is only recently that this phenomenon has been recognized as a widespread phenomenon in heterotrophic bacteria (Lamb and Dixon 1997; Buetler et al 2004; Diaz et al 2013) and phytoplankton (Marshall et al 2002, 2005; Rose et al 2008b; Schneider et al 2016; Diaz and Plummer 2018)
Summary
The reasons and mechanisms of extracellular superoxide production within marine microbes have only been minimally explored and remain unclear, a wide diversity of photoautotrophic and heterotrophic microbes have been shown to produce superoxide outside their cells under both light and dark conditions in natural waters (Rose et al 2008b; Diaz et al 2013; Hansel et al 2016). This dependence of extracellular superoxide rate to cell number is apparent regardless of whether cells are concentrated or diluted These data build upon previous studies highlighting the widespread nature of extracellular superoxide production across microbial life and provide essential rates for improved modeling of superoxide distributions within the global ocean
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