Using a systems biology approach to describe the role of dissimilatory phosphite oxidation in the global phosphorus cycle
- UC Berkeley
Overview. We investigated the role of redox reactions in the global phosphorous (P) cycle. We identified novel microbial processes responsible for oxidation of reduced phosphorous in the form of phosphite producing bioavailable phosphate. We identified central tenets that define microbial dissimilatory phosphite oxidation (DPO) and the breadth of the taxonomy of DPO microorganisms (DPOM). We demonstrated that this metabolism is vertically evolved from 3.8 GYA contemporaneously with anoxygenic phototrophy. We further demonstrate its occurrence on extant Earth as a primary mechanism driving a phosphorous redox cycle. Finally, we showed that this metabolism is environmentally maintained by the newly described autotrophic Phosphitivorax genus which rely on the reductive glycine pathway for carbon fixation. Our results demonstrate that these species are involved in a complex nutrient-dependent symbiotic relationship with their community in which they provide the fixed carbon to support the heterotrophic community and in return receive prerequisite corrinoids to maintain their activities. Intellectual Merit. P is essential for life and predominantly exists on Earth as oxidized phosphate (PO43-; P valence +5). Given the finite quantities of natural P, current unsustainable agriculture practices are predicted to deplete terrestrial reserves within ~200 years. P is critical to modern biochemical functions and can control ecosystem growth. It was presumably also important as a reagent in prebiotic chemistry. On Earth’s early surface P would have been present as a mixture of PO43- minerals, as a minor element in silicate minerals, and in reactive, reduced phases from accreted dust, meteorites, and asteroids. These sources would have weathered and plausibly furnished prebiotic Earth with abundant and potentially reactive P. The evolution of life at some point forged a P-limited biosphere, with evolutionary stress forcing the efficient extraction and recycling of P from both abiotic and biotic sources and sinks. Current P cycle models typically focus on bulk content and transport and P conversion between mineral-bound, organic, and ionic states. These models consistently overlook alternative P redox states although reduced species have been identified in diverse environments and frequently serve as a biological P source when soluble orthophosphate is limited. Phosphite (HPO32-; P valence +3), a highly soluble, geochemically stable compound, can account for up to 30% of total dissolved P in various environments. While studies suggest that life evolution may have been dependent on HPO32-, recent findings indicate an active redox cycle between PO43- and HPO32- on contemporary Earth. Currently, the extent of this cycle and its underlying processes are unknown although they impact P solubility and bioavailability. While mechanisms of PO43- reduction to HPO32- remain obscure, microbial activity is likely the principal means of HPO32- oxidation. Recently, DPO has been described in which microorganisms use HPO32- as an energy source through a largely uncharacterized metabolism. DPO may play a particularly important role in HPO32- oxidation due to the substantially higher rates and quantities of PO43- produced with this metabolism compared to biological HPO32- assimilation. Our studies demonstrate that DPO is environmentally prevalent and appears dependent on CO2 metabolism. The studies also highlighted the biochemical specialization and ancient origins of DPOM. An intricate web of nutrient sharing between DPOM and non-DPO community members is also apparent but poorly understood, putatively involving novel products of carbon fixation and corrinoids. If predictions of DPO prevalence are true, these autotrophs could serve as a key driver of primary production potentially accounting for 0.95Gt of CO2, or ~2.6% of global CO2 emissions from 2021 (36.3 Gt). Project overview. This interdisciplinary project combined geological and geochemical studies with systems biology approaches to elucidate the prevalence and constraints on P redox cycling. We investigated the natural occurrence and abundance of HPO32- in different geological settings. As part of these studies, we will investigated DPO in a broad range of environments. We uncovered the complex network of nutrient exchange and identify the existence of novel carbon reduction product(s) of this lithoautotrophic metabolism capable of sustaining heterotrophic community members as primary producers. We expect this work to shed light on how redox cycling affects the global phosphorus cycle and its integration with the carbon cycle. Broader Impacts. These studies will expand our understanding of phosphorous redox cycling in the global P cycle and its integration with the carbon cycle because DPO could additionally play an important, and heretofore unrecognized role in primary production. The importance of this work is heightened by the fact that P is an essential limiting nutrient in biological and agricultural systems and is timely given current global pressures to identify novel carbon sinks and bioavailable P resources.
- Research Organization:
- University of California, Berkeley, CA (United States)
- Sponsoring Organization:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- DOE Contract Number:
- SC0020156
- OSTI ID:
- 2324750
- Report Number(s):
- DOE-UCBERKELEY-SC0020156
- Resource Relation:
- Related Information: Supplementary Datasets S1-S9
- Country of Publication:
- United States
- Language:
- English
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