Parallel geochemical and metagenomic datasets reveal biogeochemical cycling in a hot spring ecosystem

Environmental sequence data (2,321 16S rRNA clones and 470 megabases of "metagenome" sequence) were produced from biofilms at five sites in the outflow of "Bison Pool" (BP), an alkaline hot spring in the Lower Geyser Basin of Yellowstone National Park. The outflow of BP is characterized by decreasing temperature, increasing pH, increasing dissolved oxygen, decreasing total sulfide, and changing availability of biological nutrients. Microbial life along a 22 m gradient at BP transitions from a 92°C chemotrophic streamer biofilm community in the source pool to a 56°C phototrophic mat community. Coordinated analysis of the BP Environmental Genome and a complementary contextual geochemical dataset of ~75 parameters has revealed biogeochemical cycling and metabolic and microbial community shifts within a hot spring ecosystem (1). In the BP outflow, genes diagnostic for sulfide oxidation, attributed to Aquificales in the chemosynthetic zone and Deinococcus-Thermus at the photosynthetic fringe, decrease in total number downstream. Geochemical data indicate that biological sulfide oxidation, an energy-yielding process in BP, occurs over this same range. While the genetic capacity for sulfate reduction in Thermoproteales at high temperature was found, inorganic sulfate reduction is only minimally energy-yielding at BP suggesting limited activity of these genes. Presence of apr, sat, and dsr genes in the photosynthetic mats may indicate sulfate reduction in micro-niches at depth within the biofilms, perhaps in response to increased availability of organic solutes. Carbon fixation tactics shift downstream in BP as well, as evidenced by the presence of genes associated with specific pathways and carbon isotope ratios. Capacity for the rTCA cycle, attributed to Aquificales and Thermoproteales, and the acetyl co-A pathway are found throughout BP, but are most prevalent in highest temperature sites. At lower temperature sites, fewer total carbon fixation genes were observed, perhaps indicating an increase in heterotrophic metabolism. Finally, no evidence for nitrogen fixation was found in the chemosynthetic zone at BP, corresponding to geochemical and isotopic data (3). While the capacity for partial denitrification/N-recycling was found, evidence for nitrification in the outflow is lacking. Together these datasets have allowed informed reconstruction of biogeochemical cycling and microbial community shifts in BP, and along with other recent work broaden our view of carbon fixation and nitrogen cycling in hot spring environments (2-6). 1 Swingley, W.D. et al., PLoS ONE, 7(6): e38108. 2 Hamilton, T.L., et al., 2011. EM, 13: 2204-2215. 3 Loiacono, S.T. et al., 2012. EM, 14(5): 1272-1283. 4 Steunou, A.-S. et al., 2006. PNAS, 103: 2398-2403. 5 Dodsworth, J.A. et al., 2011. EM, 13: 2371-2386. 6 Zhang, C.L. et al., 2008. AEM, 74: 6417-6426.