Dissolved organic phosphorus utilization by the marine bacterium Ruegeria pomeroyi DSS‐3 reveals chain length‐dependent polyphosphate degradation

Abstract

Summary Dissolved organic phosphorus (DOP) is a critical nutritional resource for marine microbial communities. However, the relative bioavailability of different types of DOP, such as phosphomonoesters (P‐O‐C) and phosphoanhydrides (P‐O‐P), is poorly understood. Here we assess the utilization of these P sources by a representative bacterial copiotroph, Ruegeria pomeroyi DSS‐3. All DOP sources supported equivalent growth by R. pomeroyi, and all DOP hydrolysis rates were upregulated under phosphorus depletion (−P). A long‐chain polyphosphate (45polyP) showed the lowest hydrolysis rate of all DOP substrates tested, including tripolyphosphate (3polyP). Yet the upregulation of 45polyP hydrolysis under −P was greater than any other substrate analyzed. Proteomics revealed three common P acquisition enzymes potentially involved in polyphosphate utilization, including two alkaline phosphatases, PhoD and PhoX, and one 5′‐nucleotidase (5′‐NT). Results from DOP substrate competition experiments show that these enzymes likely have broad substrate specificities, including chain length‐dependent reactivity toward polyphosphate. These results confirm that DOP, including polyP, are bioavailable nutritional P sources for R. pomeroyi, and possibly other marine heterotrophic bacteria. Furthermore, the chain‐length dependent mechanisms, rates and regulation of polyP hydrolysis suggest that these processes may influence the composition of DOP and the overall recycling of nutrients within marine dissolved organic matter.

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

“…Previous studies have shown that key marine microbes such as Synechococcus and Prochlorococcus (Moore et al, 2005), the coccolithophore Emiliania huxleyi, several Thalassiosira spp. diatoms (Diaz et al, 2016;Diaz et al, 2018;Diaz et al, 2019), and the heterotrophic bacterium Ruegeria pomeroyi (Adams et al, 2022) can grow on 3polyP as the sole P source. Here we propose that 3polyP can be utilized for both P and energy acquisition, but also that microbial interactions such as competition might control the specific exploitation of distinct DOP, reinforcing the currently accepted level of complexity of the P cycle (Duhamel et al, 2021).…”

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

“…Possessing sometimes hundreds of highly energetic phosphoanhydride bonds has also led to the suggestion that polyphosphate could be an energetically rich source of environmental energy for ancient life ( Kornberg, 1995 ; Achbergerová and Nahálka, 2011 ). 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 ).…”