Microbial genomic traits associated with phosphorus acquisition from (Fe)- complexed phytate

Abstract:

One hypothesis of why phytate persists in soils involves the strong binding of phytate to the soil solid phase or its co-precipitation with metals. Comparatively little is known about how microorganisms have evolved to access phytate under real world conditions. Here, we used a combination of soil chemical and spectroscopic analyses together with comparative genomics to connect microbial phenotypic and functional traits associated with the mobilization of metal-complexed organic phosphorous (P) in a natural ecosystem. We observed a co-localization of P and iron (Fe) concentrated at the edges of organic fragments in a P-deficient acidic soil where phytate dominated the organic fraction. This and selective extractions strongly suggested the occurrence of iron-phytate complexes in situ. Comparative genomics showed that bacteria capable of subsisting on phytate, were enriched in several potential phytate hydrolyzing enzymes. However, the ability to produce siderophores appeared to be critical for growth on Fe-complexed phytate and bacteria cultivated on insoluble iron phosphates also showed the strongest ability to hydrolyze phytate. Together this suggests that these phenotypic traits are linked. Genomic analyses showed that the biosynthetic gene clusters for siderophore production were co-located in genomes with putative phytase enzymes providing further evidence for this trait linkage. Other enriched functional traits in phytate solubilizers involved the biosynthesis of plant beneficial compounds, motility and signaling, which may contribute to rhizosphere colonization. Secretory systems, toxin-antitoxin system and antibiotic resistance genes were also prevalent and likely provide a competitive advantage to these organisms in the rhizosphere or detritusphere. In particular, type 6 secretion system (T6SS) genes were closely associated with siderophore secretion/iron transportation genes in operons, suggesting that T6SS may impart multiple fitness benefits on bacteria subsisting on Fe-complexed organic P in soils. Our work shows that soil bacteria have evolved linked functional traits to mobilize and mineralize Fe-complexed organic P that we propose is a major constraint on P turnover and availability in acidic soils.