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Abstract In the ocean, dissolved organic phosphorus (DOP) supports the health and productivity of marine phytoplankton, a phenomenon most often investigated under inorganic phosphate (Pi) scarcity. However, microbial DOP acquisition in Pi replete environments remains poorly understood. Here, we conducted a combination of nutrient addition experiments, alkaline phosphatase (AP) rate measurements, and metatranscriptomics along an onshore-to-offshore gradient in the California Current Ecosystem (CCE), an upwelling region relatively replete in Pi. We found that AP activity (APA) and eukaryotic gene transcripts for DOP utilization were present throughout the CCE. In bottle incubations, APA was upregulated in response to iron (Fe) and nitrogen (N) additions. Major contributors to these trends included atypical alkaline phosphatases (AP_aty) of diatoms in upwelling areas, and unclassified phosphodiesterases (other PDE) of multiple eukaryotic taxa in offshore regimes. APA and gene expression dynamics were not coupled to phytoplankton growth, suggesting that phytoplankton experience underlying P stress, or a state of cellular metabolism caused by Pi scarcity, even in regions primarily growth-limited by other elements. AP_atyand PDE (other) genes were highly abundant among the microbial community phosphatase pool, highlighting the importance of detecting these atypical and unclassified proteins via manual curation of metatranscriptomics data. Altogether, these results emphasize the functional diversity of phosphatases sustaining microbial community health in diverse and productive marine habitats. 

The oceanic dissolved organic phosphorus (DOP) pool is mainly composed of P-esters and, to a lesser extent, equally abundant phosphonate and P-anhydride molecules. In phosphate-limited ocean regions, diazotrophs are thought to rely on DOP compounds as an alternative source of phosphorus (P). While both P-esters and phosphonates effectively promote dinitrogen (N 2 ) fixation, the role of P-anhydrides for diazotrophs is unknown. Here we explore the effect of P-anhydrides on N 2 fixation at two stations with contrasting biogeochemical conditions: one located in the Tonga trench volcanic arc region (“volcano,” with low phosphate and high iron concentrations), and the other in the South Pacific Gyre (“gyre,” with moderate phosphate and low iron). We incubated surface seawater with AMP (P-ester), ATP (P-ester and P-anhydride), or 3polyP (P-anhydride) and determined cell-specific N 2 fixation rates, nifH gene abundance, and transcription in Crocosphaera and Trichodesmium . Trichodesmium did not respond to any DOP compounds added, suggesting that they were not P-limited at the volcano station and were outcompeted by the low iron conditions at the gyre station. Conversely, Crocosphaera were numerous at both stations and their specific N 2 fixation rates were stimulated by AMP at the volcano station and slightly by 3polyP at both stations. Heterotrophic bacteria responded to ATP and 3polyP additions similarly at both stations, despite the contrasting phosphate and iron availability. The use of 3polyP by Crocosphaera and heterotrophic bacteria at both low and moderate phosphate concentrations suggests that this compound, in addition to being a source of P, can be used to acquire energy for which both groups compete. P-anhydrides may thus leverage energy restrictions to diazotrophs in the future stratified and nutrient-impoverished ocean. 

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.