Hidden diversity and potential ecological function of phosphorus acquisition genes in widespread terrestrial bacteriophages.

Phosphorus (P) limitation of ecosystem processes is widespread in terrestrial habitats. While a few auxiliary metabolic genes (AMGs) in bacteriophages from aquatic habitats are reported to have the potential to enhance P-acquisition ability of their hosts, little is known about the diversity and potential ecological function of P-acquisition genes encoded by terrestrial bacteriophages. Here, we analyze 333 soil metagenomes from five terrestrial habitat types across China and identify 75 viral operational taxonomic units (vOTUs) that encode 105 P-acquisition AMGs. These AMGs span 17 distinct functional genes involved in four primary processes of microbial P-acquisition. Among them, over 60% (11/17) have not been reported previously. We experimentally verify in-vitro enzymatic activities of two pyrophosphatases and one alkaline phosphatase encoded by P-acquisition vOTUs. Thirty-six percent of the 75 P-acquisition vOTUs are detectable in a published global topsoil metagenome dataset. Further analyses reveal that, under certain circumstances, the identified P-acquisition AMGs have a greater influence on soil P availability and are more dominant in soil metatranscriptomes than their corresponding bacterial genes. Overall, our results reinforce the necessity of incorporating viral contributions into biogeochemical P cycling.

Remarkable effects of microbial factors on soil phosphorus bioavailability: A country-scale study.

Low soil phosphorus (P) bioavailability causes the widespread occurrence of P-limited terrestrial ecosystems around the globe. Exploring the factors influencing soil P bioavailability at large spatial scales is critical for managing these ecosystems. However, previous studies have mostly focused on abiotic factors. In this study, we explored the effects of microbial factors on soil P bioavailability of terrestrial ecosystems using a country-scale sampling effort. Our results showed that soil microbial biomass carbon (MBC) and acid phosphatase were important predictors of soil P bioavailability of agro- and natural ecosystems across China although they appeared less important than total soil P. The two microbial factors had a positive effect on soil P bioavailability of both ecosystem types and were able to mediate the effects of several abiotic factors (e.g., mean annual temperature). Meanwhile, we revealed that soil phytase could affect soil P bioavailability at the country scale via ways similar to those of soil MBC and acid phosphatase, a pattern being more pronounced in agroecosystems than in natural ecosystems. Moreover, we obtained evidence for the positive effects of microbial genes encoding these enzymes on soil P bioavailability at the country scale although their effect sizes varied between the two ecosystem types. Taken together, this study demonstrated the remarkable effects of microbial factors on soil P bioavailability at a large spatial scale, highlighting the importance to consider microbial factors in managing the widespread P-limited terrestrial ecosystems.

A comprehensive synthesis unveils the mysteries of phosphate-solubilizing microbes.

Phosphate-solubilizing microbes (PSMs) drive the biogeochemical cycling of phosphorus (P) and hold promise for sustainable agriculture. However, their global distribution, overall diversity and application potential remain unknown. Here, we present the first synthesis of their biogeography, diversity and utility, employing data from 399 papers published between 1981 and 2017, the results of a nationwide field survey in China consisting of 367 soil samples, and a genetic analysis of 12986 genome-sequenced prokaryotic strains. We show that at continental to global scales, the population density of PSMs in environmental samples is correlated with total P rather than pH. Remarkably, positive relationships exist between the population density of soil PSMs and available P, nitrate-nitrogen and dissolved organic carbon in soil, reflecting functional couplings between PSMs and microbes driving biogeochemical cycles of nitrogen and carbon. More than 2704 strains affiliated with at least nine archaeal, 88 fungal and 336 bacterial species were reported as PSMs. Only 2.59% of these strains have been tested for their efficiencies in improving crop growth or yield under field conditions, providing evidence that PSMs are more likely to exert positive effects on wheat growing in alkaline P-deficient soils. Our systematic genetic analysis reveals five promising PSM genera deserving much more attention.