Tight Regulation of Extracellular Superoxide Points to Its Vital Role in the Physiology of the Globally Relevant <italic toggle="yes">Roseobacter</italic> Clade

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 remai...

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Autores principales:	Colleen M. Hansel, Julia M. Diaz, Sydney Plummer
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Roseobacter reactive oxygen species superoxide superoxide dismutase Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/e701e5f8cb0648ffa03223eb958f2f17
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spelling	oai:doaj.org-article:e701e5f8cb0648ffa03223eb958f2f172021-11-15T15:55:25ZTight Regulation of Extracellular Superoxide Points to Its Vital Role in the Physiology of the Globally Relevant <italic toggle="yes">Roseobacter</italic> Clade10.1128/mBio.02668-182150-7511https://doaj.org/article/e701e5f8cb0648ffa03223eb958f2f172019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02668-18https://doaj.org/toc/2150-7511ABSTRACT 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.Colleen M. HanselJulia M. DiazSydney PlummerAmerican Society for MicrobiologyarticleRoseobacterreactive oxygen speciessuperoxidesuperoxide dismutaseMicrobiologyQR1-502ENmBio, Vol 10, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Roseobacter reactive oxygen species superoxide superoxide dismutase Microbiology QR1-502
spellingShingle	Roseobacter reactive oxygen species superoxide superoxide dismutase Microbiology QR1-502 Colleen M. Hansel Julia M. Diaz Sydney Plummer Tight Regulation of Extracellular Superoxide Points to Its Vital Role in the Physiology of the Globally Relevant <italic toggle="yes">Roseobacter</italic> Clade
description	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.
format	article
author	Colleen M. Hansel Julia M. Diaz Sydney Plummer
author_facet	Colleen M. Hansel Julia M. Diaz Sydney Plummer
author_sort	Colleen M. Hansel
title	Tight Regulation of Extracellular Superoxide Points to Its Vital Role in the Physiology of the Globally Relevant <italic toggle="yes">Roseobacter</italic> Clade
title_short	Tight Regulation of Extracellular Superoxide Points to Its Vital Role in the Physiology of the Globally Relevant <italic toggle="yes">Roseobacter</italic> Clade
title_full	Tight Regulation of Extracellular Superoxide Points to Its Vital Role in the Physiology of the Globally Relevant <italic toggle="yes">Roseobacter</italic> Clade
title_fullStr	Tight Regulation of Extracellular Superoxide Points to Its Vital Role in the Physiology of the Globally Relevant <italic toggle="yes">Roseobacter</italic> Clade
title_full_unstemmed	Tight Regulation of Extracellular Superoxide Points to Its Vital Role in the Physiology of the Globally Relevant <italic toggle="yes">Roseobacter</italic> Clade
title_sort	tight regulation of extracellular superoxide points to its vital role in the physiology of the globally relevant <italic toggle="yes">roseobacter</italic> clade
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/e701e5f8cb0648ffa03223eb958f2f17
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Tight Regulation of Extracellular Superoxide Points to Its Vital Role in the Physiology of the Globally Relevant <italic toggle="yes">Roseobacter</italic> Clade

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