Contrasting Roles of DOP as a Source of Phosphorus and Energy for Marine Diazotrophs

Abstract

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 (N2) fixation, the role of P-anhydrides for diazotrophs is unknown. Here we explore the effect of P-anhydrides on N2 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 N2 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 N2 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.

Natural iron fertilization by shallow hydrothermal sources fuels diazotroph blooms in the ocean

“…This peak in diazotroph activity was marked by a phosphate drawdown (~50 nM) in the photic layer, although concentrations were not limiting for Trichodesmium spp. ( 27 ) because of intense microbial phosphorus cycling in this region ( 28 ). Diazotrophs were favored by the extremely low nitrate concentrations along the transect (fig.…”

Dissolved organic matter offsets the detrimental effects of climate change in the nitrogen‐fixing cyanobacterium Crocosphaera

“…Furthermore, despite the competitiveness of Crocosphaera against other community components for these labile substrates is unknown, this diazotroph shows significant uptake of organic carbon derived from a mixture of representative natural carbohydrates and amino acids (see Supporting Information). Diazotrophic cyanobacteria may use DOM as an alternative source of carbon, nutrients and/or energy (Dhyrman et al 2006;Filella et al 2022), for example Trichodesmium can obtain as much carbon from amino acids as from DIC (Benavides et al 2017). In contrast, the non-diazotrophic cyanobacterium Prochlorococcus obtains more carbon from DIC than from DOM uptake but can assimilate glucose in culture and field conditions (Moisander et al 2012;Muñoz-Marín et al 2013;Duhamel et al 2018).…”

“…Trichodesmium and Crocosphaera are able to use phosphoesters (Dyhrman et al 2002;Orchard et al 2003), but only Trichodesmium obtains phosphorus from phosphonates (Dyhrman et al 2006). Crocosphaera can obtain both phosphorus and energy from phosphoanhydrides (Filella et al 2022). These studies point toward an overlooked role of osmotrophy, the uptake of DOM, for cyanobacteria survival in the future ocean.…”

On the potential roles of phosphorus in the early evolution of energy metabolism

“…Today, certain marine microorganisms are able to consume environmental polyphosphates as their sole source of phosphorus for growth and may even prefer polyphosphates over typical sources of biological phosphorus, although it remains unknown how widespread this recently discovered metabolic trait is ( Diaz et al, 2018 , 2019 ; Adams et al, 2022 ). It is hypothesized that microbes could be utilizing polyphosphates as an environmental source of energy, not just phosphorus, due to the catabolism of polyphosphate under non-limited phosphorus conditions ( Peck et al, 1983 ; Filella et al, 2022 ). It has also been suggested that the prokaryotic PPK1 enzyme evolved after PPK2, indicating that degradation of polyphosphates could be older than synthesis.…”