Freshwater microbial phosphorus metabolism: analysis of metagenome and bacterial isolates from the ultraoligotrophic Lake Matano

Date
2016
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University of Delaware
Abstract
Phosphorus (P) is a fundamental macronutrient for all living organisms since it is a component of DNA, RNA, phospholipids, adenosine triphosphate (ATP) and other P containing proteins. However, P is limited in many natural systems, including soil, freshwater and marine environments, which affects the primary and heterotrophic bacterial productivity. Lake Matano, located in South Sulawesi Island, Indonesia, is an ultra-oligotrophic, ferruginous (iron rich), and tropical lake. The P concentration in the surface water is below 50 nM, and most of the P in the lake is adsorbed by iron (hydr)oxides coming from the high iron content soil of the catchment basin. The P in the deeper water and sediment is not available to the surface water because the lake is permanently stratified. The surface water is chronically P-limited and thus a good study site for P limitation responses. ☐ Here, we use a metagenomic data set of the microbial community from Lake Matano surface water and the heterotrophic bacteria isolated from the same depth of water (10 m) to study the microbial responses to P limitation and their ecological consequences. Metagenomic analysis showed that the high-affinity phosphate specific transport (Pst) genes, alkaline phosphatase genes, phosphonate cleavage genes, and polyphosphate metabolism genes are enriched in the surface water compared to the Clusters of Orthologous Groups (COG) database. The phosphite dehydrogenase (PtxD) which can oxidize phosphite to Pi is also abundant in the metagenomic data set. ☐ Seven heterotrophic bacteria were isolated from the surface water, and they can grow without additional P, although very slowly. In response to P limitation, they can reduce their P requirements by reducing their RNA contents and by substituting their phospholipids with P-free lipids. They can also utilize diverse P sources, including P compounds with oxidation state of +5 (inorganic phosphate (Pi) and organophosphate esters), P compounds with oxidation state of +3 (methylphosphonate, 2-aminoethylphosphonate, and phosphite), and insoluble mineral-associated P complexes (hydroxyapatite, and complex of hydrous ferric oxides and Pi (HFO-P)). The isolate LM-Y can solubilize more Pi from the mineral-associated P i than its requirement, resulting in high Pi concentration in the supernatant of the culture. Most of the P in Lake Matano is adsorbed by iron (hydr)oxides, Pi solubilizing bacteria can solubilize P i from the iron (hydr)oxides to support the growth of themselves and other organisms in the same environment. The use of MPn as P source by four isolates produced methane, which might contribute to the excess methane in the oxic surface water of Lake Matano. Addition of Pi into the MPn containing medium inhibited the methane production. The transcript levels of phnJ gene, which encodes the enzyme that cleaves C-P bond in the intermediate alpha-D-ribose-1-methylphosphonate-5-phosphate to release methane, were higher in the medium with only MPn and lower in the medium with both MPn and P i.
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