Superoxide production by marine microalgae

Marshall, Judith-Anne; Ross, Tom; Pyecroft, Stephen; Hallegraeff, Gustaaf M.

doi:10.1007/s00227-005-1597-6

Cited by 82 publications

(38 citation statements)

References 20 publications

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“…S3; Diaz et al 2013). Similarly, a complex relationship was previously observed between cell density and the superoxide produced per cell for C. marina and the prymnesiophyte alga Prymnesium parvum (Marshall et al 2005). Below 10,000 C. marina cells, cell-normalized superoxide production rates increased with cell density.…”

Section: Discussionsupporting

confidence: 64%

“…However, above this density, an inverse relationship was observed for cell density and superoxide produced per cell. Furthermore, serial dilution of both medium-and high-density C. marina cultures resulted in significantly increased cell normalized superoxide production levels and production rates following 1 h of incubation (Marshall et al 2005).…”

Section: Discussionmentioning

confidence: 95%

“…ROS, particularly superoxide, are also produced extracellularly by a broad range of microorganisms, including fungi, phytoplankton, and bacteria (Aguirre et al 2005;Kustka et al 2005;Marshall et al 2005;Rose et al 2008b;Learman et al 2011;Hansel et al 2012;Rose 2012;Diaz et al 2013;Tang et al 2013). Research in the past decade has introduced phytoplankton and, most recently, heterotrophic bacteria as significant sources of ROS, including superoxide.…”

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confidence: 99%

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Dynamics of extracellular superoxide production by Trichodesmium colonies from the Sargasso Sea

Hansel

Buchwald

Diaz

et al. 2016

Limnology & Oceanography

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Reactive oxygen species (ROS) are key players in the health and biogeochemistry of the ocean and its inhabitants. The vital contribution of microorganisms to marine ROS levels, particularly superoxide, has only recently come to light, and thus the specific biological sources and pathways involved in ROS production are largely unknown. To better understand the biogenic controls on ROS levels in tropical oligotrophic systems, we determined rates of superoxide production under various conditions by natural populations of the nitrogen-fixing diazotroph Trichodesmium obtained from various surface waters in the Sargasso Sea. Trichodesmium colonies collected from eight different stations all produced extracellular superoxide at high rates in both the dark and light. Colony density and light had a variable impact on extracellular superoxide production depending on the morphology of the Trichodesmium colonies. Raft morphotypes showed a rapid increase in superoxide production in response to even low levels of light, which was not observed for puff colonies. In contrast, superoxide production rates per colony decreased with increasing colony density for puff morphotypes but not for rafts. These findings point to Trichodesmium as a likely key source of ROS to the surface oligotrophic ocean. The physiological and/or ecological factors underpinning morphology-dependent controls on superoxide production need to be unveiled to better understand and predict superoxide production by Trichodesmium and ROS dynamics within marine systems.

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Section: Discussionsupporting

confidence: 64%

Section: Discussionmentioning

confidence: 95%

mentioning

confidence: 99%

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Dynamics of extracellular superoxide production by Trichodesmium colonies from the Sargasso Sea

Hansel

Buchwald

Diaz

et al. 2016

Limnology & Oceanography

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“…Biological production of

O_{2}^{- *}

in the extracellular milieu has been reported from culture studies involving a wide range of environmentally occurring aquatic microorganisms, including eukaryotic microalgae from the class Raphidophyceae (Oda et al, 1997; Marshall et al, 2002, 2005; Yamasaki et al, 2004; Garg et al, 2007a); dinoflagellates and prymnesiophytes (Yamasaki et al, 2004; Marshall et al, 2005); marine diatoms from the genus Thalassiosira (Kustka et al, 2005); marine cyanobacteria from the genera Synechococcus (Rose et al, 2008b), Lyngbya (Rose et al, 2005) and Trichodesmium (Godrant et al, 2009); a marine alphaproteobacterium from the genus Roseobacter (Learman et al, 2011); the freshwater cyanobacterium Microcystis aeruginosa (Fujii et al, 2011); the unicellular protozoan coral symbiont Symbiodinium (Saragosti et al, 2010); fungi and yeasts including Aspergillus nidulans (Lara-Ortíz et al, 2003) and Saccharomyces cerevisiae (Shatwell et al, 1996), as reviewed by Aguirre et al (2005); and the heterotrophic bacteria Paracoccus denitrificans (Henry and Vignais, 1980) and Escherichia coli (Korshunov and Imlay, 2006). Rates of ESP vary enormously between these different organisms, with the maximum reported rates being from the marine Raphidophycean Chattonella marina of up to ∼5 pmol cell −1 h −1 (Oda et al, 1997; Garg et al, 2007a).…”

Section: Sources Of Extracellular Superoxide In Natural Watersmentioning

confidence: 99%

The Influence of Extracellular Superoxide on Iron Redox Chemistry and Bioavailability to Aquatic Microorganisms

Rose¹

2012

Front. Microbio.

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Superoxide, the one-electron reduced form of dioxygen, is produced in the extracellular milieu of aquatic microbes through a range of abiotic chemical processes and also by microbes themselves. Due to its ability to promote both oxidative and reductive reactions, superoxide may have a profound impact on the redox state of iron, potentially influencing iron solubility, complex speciation, and bioavailability. The interplay between iron, superoxide, and oxygen may also produce a cascade of other highly reactive transients in oxygenated natural waters. For microbes, the overall effect of reactions between superoxide and iron may be deleterious or beneficial, depending on the organism and its chemical environment. Here I critically discuss recent advances in understanding: (i) sources of extracellular superoxide in natural waters, with a particular emphasis on microbial generation; (ii) the chemistry of reactions between superoxide and iron; and (iii) the influence of these processes on iron bioavailability and microbial iron nutrition.

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“…In sunlit and dark waters alike, microbes appear to be prolific producers of extracellular superoxide (Rose et al 2008b;Diaz et al 2013;Hansel et al 2016;Schneider et al 2016). The diversity of microorganisms contributing to the oceanic superoxide flux is just beginning to come to light with a broad taxonomic representation already evident (Kustka et al 2005;Marshall et al 2005;Rose et al 2008b;Learman et al 2011;Diaz et al 2013Diaz et al , 2016Hansel et al 2016;Zhang et al 2016b;.…”

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confidence: 99%

Extracellular superoxide production by key microbes in the global ocean

Sutherland

Coe

Gast

et al. 2019

Limnology & Oceanography

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Bacteria 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.

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Superoxide production by marine microalgae

Cited by 82 publications

References 20 publications

Dynamics of extracellular superoxide production by Trichodesmium colonies from the Sargasso Sea

Dynamics of extracellular superoxide production by Trichodesmium colonies from the Sargasso Sea

The Influence of Extracellular Superoxide on Iron Redox Chemistry and Bioavailability to Aquatic Microorganisms

Extracellular superoxide production by key microbes in the global ocean

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