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Abstract Dissolved organic phosphorus (DOP) contains compounds with phosphoester, phosphoanhydride, and phosphorus–carbon bonds. While DOP holds significant nutritional value for marine microorganisms, the bioavailability of each bond-class to the widespread cyanobacterium Synechococcus remains largely unknown. This study evaluates bond-class specific DOP utilization by Synechococcus strains from open and coastal oceans. Both strains exhibited comparable growth rates when provided phosphate, a phosphoanhydride [3-polyphosphate and 45-polyphosphate], or a DOP compound with both phosphoanhydride and phosphoester bonds (adenosine 5′-triphosphate). Growth rates on phosphoesters [glucose-6-phosphate, adenosine 5′-monophosphate, bis(4-methylumbelliferyl) phosphate] were variable, and neither strain grew on selected phosphorus–carbon compounds. Both strains hydrolyzed 3-polyphosphate, then adenosine 5′-triphosphate, and lastly adenosine 5′-monophosphate, exhibiting preferential enzymatic hydrolysis of phosphoanhydride bonds. The strains’ exoproteomes contained phosphorus hydrolases, which combined with enhanced cell-free hydrolysis of 3-polyphosphate and adenosine 5′-triphosphate under phosphate deficiency, suggests active mineralization of phosphoanhydride bonds by these exoproteins. Synechococcus alkaline phosphatases presented broad substrate specificities, including activity toward the phosphoanhydride 3-polyphosphate, with varying affinities between strains. Collectively, these findings underscore the potentially significant role of compounds with phosphoanhydride bonds in Synechococcus phosphorus nutrition and highlight varied growth and enzymatic responses to molecular diversity within DOP bond-classes, thereby expanding our understanding of microbially mediated DOP cycling in marine ecosystems.
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This content will become publicly available on April 9, 2026
Atypical phosphatases drive dissolved organic phosphorus utilization by phosphorus-stressed phytoplankton in the California Current Ecosystem
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 (APaty) 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. APatyand 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.
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- Award ID(s):
- 2224726
- PAR ID:
- 10598539
- Publisher / Repository:
- bioRxiv
- Date Published:
- Format(s):
- Medium: X
- Institution:
- bioRxiv
- Sponsoring Org:
- National Science Foundation
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