Holden, Stewart

White Paper Title: 
Hydrogen limits on growth and maintenance energy estimates for thermophiles and hyperthermophiles

James F. Holden and Lucy C. Stewart
Department of Microbiology, University of Massachusetts, Amherst, MA 01003

We are interested in biogeochemical processes in deep-sea hydrothermal systems and can contribute to the integration and synthesis of ideas related to in situ bioenergetics and habitat modeling. At appropriate temperatures and pHs, life exists where the metabolic energy available for growth exceeds the maintenance energy costs of living in that environment. Existing bioenergetic models have little data for metabolic processes above 50°C, some key modeling assumptions require refinement, and the physiological bases for maintenance energy variations in thermophiles needs study. Our field and laboratory work with hyperthermophilic methanogens from the Endeavour Segment and Axial Volcano on the Juan de Fuca Ridge shows that they are H2 limited below 10-20 µM, which generally explains their distribution patterns at several global vent sites. H2 deficits are compensated for through commensal growth with H2 producing hyperthermophilic heterotrophs that likely obtain their energy from nearby mesophilic sources. In pure culture studies, CH4 production rates per cell increase significantly towards the physical and chemical limits of their growth suggesting that maintenance energies vary within an organism with environmental conditions that must be accounted for in habitat models. These data are needed to model biogeochemical processes such as CO2 fixation in the deep sea, sulfur and metal fluxes, and carbon and nitrogen flow through trophic levels.

Modeling the bioenergetics of metabolism above 50°C requires a better understanding of maintenance energy costs that will require the input of microbiologists, fluid geochemists, and bioenergetic modelers. Our future research includes studying thermophiles and hyperthermophiles with varying metabolisms to measure maintenance energy costs, account for differences in these costs due to physiology, and ground truth our laboratory findings with field studies. Another goal is to concomitantly analyze the metabolites of these organisms using RAMAN-LIBS to establish biosignatures for in situ sensor development.