Microbial heterotrophic production in an oligotrophic acidic geothermal lake: responses to organic amendments and terrestrial plant litter

Abstract

Boiling Springs Lake (BSL) is an oligotrophic, acidic geothermal feature where even very low levels of microbial heterotrophic production still exceed autotrophy. To test whether allochthonous leaf litter (LL) inputs fuel this excess, we quantified leaf litterfall, leaching and decomposition kinetics, and measured the impact of organic amendments on production, germination and cell growth, using pyrosequencing to track changes in microbial community composition. Coniferous leaves in BSL exhibited high mass loss rates during leaching and decomposition, likely due to a combination of chemical hydrolysis and contributions of both introduced and endemic microbes. We measured very low in situ (3)H-thymidine incorporation over hours by the dominant chemolithotroph Acidimicrobium (13-65 μg C L(-1) day(-1)), which was inhibited by simple C sources (acetate, glucose). Longer term incubations with additions of 0.01-0.02% complex C/N sources induced germination of the Firmicute Alicyclobacillus within 1-2 days, as well as growth of Acetobacteraceae after 3-4 days. LL additions yielded the opposite successional patterns of these r-selected heterotrophs, boosting production to 30-150 μg C L(-1) day(-1). Growth and germination studies suggest both prokaryotes and fungi likely consume allochthonous organics, and might be novel sources of lignocellulose-degrading enzymes. A model of BSL's C budget supports the hypothesis that allochthonous inputs fuel seasonal microbial heterotrophy, but that dissolved organic C sources greatly exceed direct LL inputs.

Keywords: C cycle; allochthonous inputs; biogeochemistry; extreme environments; heterotrophic production.