TY - JOUR
T1 - Dissolved organic phosphorus utilization by the marine bacterium Ruegeria pomeroyi DSS-3 reveals chain length-dependent polyphosphate degradation
AU - Adams, Jamee C.
AU - Steffen, Rachel
AU - Chou, Chau Wen
AU - Duhamel, Solange
AU - Diaz, Julia M.
N1 - Funding Information:
The authors acknowledge Alisia Holland for contributing to the development of culturing methods during an early stage of this project. This work was supported by the National Science Foundation under grants 1737083, 2001212 (S.D.), 1736967, 1948042 (J.M.D.), 1737240 (S.D.), 1559124 and 2015310 (J.M.D.), as well as the Simons Foundation under grant 678537 (J.M.D.) and the Sloan Foundation (J.M.D.). The raw data supporting the conclusions of this manuscript are deposited at the Biological and Chemical Oceanography Data Management Office (http://bco-dmo.org) under project number 747715.
Funding Information:
The authors acknowledge Alisia Holland for contributing to the development of culturing methods during an early stage of this project. This work was supported by the National Science Foundation under grants 1737083, 2001212 (S.D.), 1736967, 1948042 (J.M.D.), 1737240 (S.D.), 1559124 and 2015310 (J.M.D.), as well as the Simons Foundation under grant 678537 (J.M.D.) and the Sloan Foundation (J.M.D.). The raw data supporting the conclusions of this manuscript are deposited at the Biological and Chemical Oceanography Data Management Office ( http://bco-dmo.org ) under project number 747715.
Publisher Copyright:
© 2022 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.
PY - 2022
Y1 - 2022
N2 - 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.
AB - 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.
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U2 - 10.1111/1462-2920.15877
DO - 10.1111/1462-2920.15877
M3 - Article
AN - SCOPUS:85123951316
JO - Environmental Microbiology
JF - Environmental Microbiology
SN - 1462-2912
ER -