Timing the Evolution of Phosphorus-Cycling Enzymes Through Geological Time

Abstract

SUMMARY PARAGRAPHPhosphorus plays a crucial role in controlling biological productivity, but geological estimates of phosphate concentrations in the Precambrian ocean, during life’s origin and early evolution, vary over several orders of magnitude1-10. While reduced phosphorus species may have served as alternative substrates to phosphate11, their bioavailability on the early Earth remains unknown. Here, we reconstruct the phylogenomic record of life on Earth and find that phosphate transporting genes (pnas) evolved in the mid-Archean (ca. 3.2 Ga) and are consistent with phosphate concentrations above modern levels (>3 μM). The first gene optimized for low phosphate levels (pstS; <1 μM) appeared around 2.9 Ga. Most enzymatic pathways for metabolising reduced phosphorus emerged and expanded across the tree of life in the Neoarchean to Paleoproterozoic (ca. 2.6 to 1.8 Ga). This includes phosphonate-catabolising CP-lyases, phosphite-oxidising pathways and hypophosphite-oxidising pathways. CP-lyases are particularly abundant in dissolved phosphate concentrations below 0.1 μM. Our results thus indicate declining phosphate levels through the Archean, possibly linked to increasing deposition of phosphate-scavenging iron oxides, which may have limited productivity. However, reduced phosphorus species did not become widely used until after the Paleoproterozoic Great Oxidation Event (2.3 Ga), possibly linked to an expansion of the biosphere at that time.