Tight regulation of extracellular superoxide points to its vital role in the physiology of the globally relevant Roseobacter clade.
Citable URI
https://hdl.handle.net/1912/23981As published
https://doi.org/10.1128/mBio.02668-18DOI
10.1128/mBio.02668-18Abstract
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.
Description
© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Hansel, C. M., Diaz, J. M., & Plummer, S.. Tight regulation of extracellular superoxide points to its vital role in the physiology of the globally relevant Roseobacter clade. Mbio, 10(2), (2019):e02668-18, doi:10.1128/mBio.02668-18.
Collections
Suggested Citation
Hansel, C. M., Diaz, J. M., & Plummer, S. (2019). Tight regulation of extracellular superoxide points to its vital role in the physiology of the globally relevant Roseobacter clade. Mbio, 10(2), e02668-18.The following license files are associated with this item:
Related items
Showing items related by title, author, creator and subject.
-
Environmental sensing and response genes in cnidaria : the chemical defensome in the sea anemone Nematostella vectensis
Goldstone, Jared V. (2008-10)The starlet sea anemone Nematostella vectensis has been recently established as a new model system for the study of the evolution of developmental processes, as cnidaria occupy a key evolutionary position at the base of ... -
The presence of four iron-containing superoxide dismutase isozymes in Trypanosomatidae : characterization, subcellular localization, and phylogenetic origin in Trypanosoma brucei
Dufernez, Fabienne; Yernaux, Cedric; Gerbod, Delphine; Noel, Christophe; Chauvenet, Melanie; Wintjens, Rene; Edgcomb, Virginia P.; Capron, Monique; Opperdoes, Fred R.; Viscogliosi, Eric (2005-08-11)Metalloenzymes such as the superoxide dismutases (SODs) form part of a defense mechanism that helps protect obligate and facultative aerobic organisms from oxygen toxicity and damage. Here, we report the presence in the ... -
Dark production of extracellular superoxide by the coral Porites astreoides and representative symbionts
Zhang, Tong; Diaz, Julia M.; Brighi, Caterina; Parsons, Rachel J.; McNally, Sean; Apprill, Amy; Hansel, Colleen M. (Frontiers Media, 2016-11-24)The reactive oxygen species (ROS) superoxide has been implicated in both beneficial and detrimental processes in coral biology, ranging from pathogenic disease resistance to coral bleaching. Despite the critical role of ...