Global and seasonal variation of marine phosphonate metabolism

Abstract

Marine microbial communities rely on dissolved organic phosphorus (DOP) remineralisation to meet phosphorus (P) requirements. We extensively surveyed the genomic and metagenomic distribution of genes directing phosphonate biosynthesis, substrate-specific catabolism of 2-aminoethylphosphonate (2-AEP, the most abundant phosphonate in the marine environment), and broad-specificity catabolism of phosphonates by the C-P lyase (including methylphosphonate, a major source of methane). We developed comprehensive enzyme databases by curating publicly available sequences and then screened metagenomes from TARA Oceans and Munida Microbial Observatory Time Series (MOTS) to assess spatial and seasonal variation in phosphonate metabolism pathways. Phosphonate cycling genes were encoded in diverse gene clusters by 35 marine bacterial and archaeal classes. More than 65% of marine phosphonate cycling genes mapped to Proteobacteria with production demonstrating wider taxonomic diversity than catabolism. Hydrolysis of 2-AEP was the dominant phosphonate catabolism strategy, enabling microbes to assimilate carbon and nitrogen alongside P. Genes for broad-specificity catabolism by the C-P lyase were far less widespread, though enriched in the extremely P-deplete environment of the Mediterranean Sea. Phosphonate cycling genes were abundant in marine metagenomes, particularly from the mesopelagic zone and winter sampling dates. Disparity between prevalence of substrate-specific and broad-specificity catabolism may be due to higher resource expenditure from the cell to build and retain the C-P lyase. This study is the most comprehensive metagenomic survey of marine microbial phosphonate cycling to date and provides curated databases for 14 genes involved in phosphonate cycling.

Taxonomic distribution of metabolic functions underpins nutrient cycling inTrichodesmiumconsortia

“…Nonetheless, the presence of a broad- specificity C-P lyase appeared to be the most prevalent strategy for phosphonate utilization within the Trichodesmium consortium. This finding is in contrast to a meta-analysis of marine metagenomes where the most common phosphonate degradation strategy within the water column was the substrate-specific hydrolysis of 2-AEP (54). 2-AEP is the most abundant phosphonate source in the marine environment (55), and the differences in enzyme distribution within the Trichodesmium consortium may reflect heterogeneity in the phosphonate compounds present in the colony, relative to the water column.…”

A mutant fitness assay identifies bacterial interactions in a model ocean hot spot

“…Despite the phosphate-replete medium, fitness decrease of a phosphonate utilization mutant ( phnM ) suggested an increased reliance on dissolved organic phosphate. Genomic analysis indicated that R. pomeroyi is the only bacterium in the model phycosphere communities with a broad-specificity C-P lyase, suggesting another niche dimension that could decrease direct competition ( 33 ) ( SI Appendix , Table S1 ). Fitness decreases in multispecies communities were observed for mutants of polyphosphate kinase ( ppk ) which are unable to utilize stored polyphosphate, an energetically economical source of phosphorous for ATP ( 34 ).…”

Population genomics of Australian indigenous Mesorhizobium reveals diverse nonsymbiotic genospecies capable of nitrogen-fixing symbioses following horizontal gene transfer

“…Despite lacking the many genes required for symbiosis, ICE M sp B4-1-4 was larger than the median length for tripartite ICESyms (~560 kb) at 626 kb. ICE M sp B4-1-4 carried two gene clusters likely involved in the broad-specificity catabolism of phosphonates [ 74 ] and a plethora of metabolic enzymes with predicted involvement in fatty acid degradation, metabolism of butanoate, aspartate, asparagine, glutamate and proline.…”