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

Abstract

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.

Species-specific control of external superoxide levels by the coral holobiont during a natural bleaching event

“…For example, according to a recent study, corals may release external hydrogen peroxide to facilitate feeding on zooplankton or as a mode of defence against pathogens regulated by physical and chemical stimuli67. Consistent with the ability of superoxide to act as a cell density-dependent growth promoter, and with previous observations from phytoplankton and heterotrophic bacteria68, we found that extracellular superoxide production by actively developing coral larvae was inversely related to larval density (Supplementary Fig. 3).…”

Extracellular superoxide production by key microbes in the global ocean

“…Despite a widespread ability of marine microbes to produce extracellular superoxide, the reasons for this process and underlying mechanisms remain unclear. Extracellular superoxide production rates are dependent upon physiological and environmental factors, such as cell growth stage, cell density, light intensity, iron availability, and overall nutrient availability (Rose et al ; Diaz et al , ; Hansel et al ; Schneider et al ; Hansel et al ). The data we present in this study expand the number of organisms known to display cell‐density–dependent superoxide production to include additional eukaryotic algae, picocyanobacteria, and picobacteria.…”

“…Previous work has shown that these photosynthetic organisms may produce significant internal ROS from light‐dependent processes, but we show here that these organisms are also prolific producers of superoxide in the dark. Furthermore, light has been shown to increase extracellular superoxide levels by some phytoplankton (Hansel et al ; Schneider et al ; Zhang et al ; Diaz et al ), suggesting that these organisms may be even greater sources of marine superoxide, depending on prevailing light conditions. The significant superoxide flux suggested by our measurements has further implications on trace nutrient cycling within the ocean.…”

“…All measurements, including calibrations, were collected under dark conditions, which were maintained by covering sample tubing and filter with aluminum foil. Similar systems have been used to generate high‐sensitivity measurements of natural superoxide concentrations and decay rates (Rose et al ; Hansard et al ), as well as extracellular superoxide production by bacteria (Diaz et al ), phytoplankton isolates (Kustka et al ; Rose et al ), and natural Trichodesmium colonies (Hansel et al ).…”

N2 fixation in free‐floating filaments of Trichodesmium is higher than in transiently suboxic colony microenvironments

“…Lesser, ). In line with this, high superoxide production by field‐collected Trichodesmium colonies has been observed (Hansel et al ., ). Accumulation of O 2 and reactive oxygen species in the colony microenvironment may therefore increase the risk of oxidative stress in colonies compared with single trichomes and might be part of the reason why colonies showed lower N 2 and C fixation rates.…”