Microbially-mediated carbon and nitrogen cycling in hydrocarbon-based ecosystems
The biologically-mediated formation of methane (methanogenesis) is an important process in many terrestrial and oceanic anaerobic environments, and is the largest source of methane on the planet (Reeburgh, 1996). It has long been suggested that in anaerobic environments, methanogenesis is a terminal step in ecological carbon flow, and constitutes the largest carbon sink in many of these environments (Zinder, 1993). However, in the last twenty-five years there has been compelling evidence that microbially-mediated anaerobic methane oxidation (AMO) is also a major form of carbon cycling in marine environments (Valentine et al, 2000). AMO is potentially widespread, and may be responsible for consuming much of the methane, ca. 5-20% of the methane flux per year, that is currently unaccounted for in global methane budgets (Reeburgh and Alperin, 1988). Currently, there are two groups of archaea (ANME-1 and ANME-2), closely related to methanogens, that have been shown to be involved in the anaerobic oxidation of methane in marine sediments (Hinrichs, et al 1999; Boetius et al, Orphan et al, 2001a,b, 2002). However, the metabolic pathways mediating this process remain enigmatic, the environmental factors that influence AMO are not well established, and the fine-scale distribution and abundance of microorganisms catalyzing AMO are largely unknown. These archaea have yet to be recovered in pure culture, and many key aspects of the ecology and physiology of anaerobic methanotrophs remain poorly understood, in particular the population growth rates and the influence of environmental factors on the distribution and abundance of the known anaerobic methanotrophic groups.
Recently, I developed a unique continuous flow bioreactor known as AMIS that has been shown to support the growth and enrichment of anaerobic methanotrophic archaea in the laboratory.
With my colleagues, we have been conducting experiments to better understand the potential growth rates of ANME-1 and ANME-2 methanotrophs, and to examine the influence of sediment advective flow rates on the distribution and abundance of these methanotrophs. We are also exploring the role of anaerobic methanotrophs in carbon and nitrogen cycling at hydrothermal vents.
Chemoautotrophic symbioses are often the dominant macrofauna at hydrothermal vents. Riftia pachyptila, a vestimentiferan tubeworm, flourishes at hydrothermal vent along the East Pacific (Jones 1981, Hessler 1984). Devoid of a mouth or digestive tract, it relies on chemoautotrophic symbionts (that are housed in host bacteriocytes deep within the worm) for nourishment. Riftia pachyptila is believed to be one of the fastest growing metazoans (Lutz et al, 1994), a feat accomplished without significant heterotrophic nutrient acquisition. The observed tremendous growth rates suggest that the symbionts have high rates of chemoautotrophic metabolism and require that the host maintain sufficient influx of metabolites and efflux of end products to sustain chemoautotrophic metabolism.
My research has shown that Riftia pachyptila can acquire carbon dioxide from the environment at rates that can support very high growth rates, up to 7.9% total body carbon per day. The oxidation of sulfide by the symbionts requires oxygen, not nitrate, and is responsible for the production of protons. Because Riftia pachyptila relies on a pH gradient between the internal milieu and the environment to sustain inorganic carbon acquisition for chemoautotrophic carbon fixation, the rapid elimination of protons is critical to sustaining carbon fixation. My research has also shown that proton elimination by Riftia pachyptila sustains inorganic carbon uptake, and that Riftia pachyptila proton elimination rates are the highest recorded to date. Nitrate acquisition by Riftia pachyptila and the symbiotic reduction to ammonia is the source of nitrogen for this association, and is sufficient to sustain the observed growth rates of Riftia pachyptila.
In concert, these findings demonstrate that the tight physiological coupling between the Riftia pachyptila host and symbionts supports the very high rates of chemoautotrophic function. Because metabolite availability in the vent environment is temporally variable, the ability of Riftia pachyptila to rapidly acquire the necessary metabolites when available (as well eliminate the chemoautotrophic end products), is essential to maintaining the observed high growth rates. The dominance of Riftia pachyptila at many hydrothermal vents is likely attributable to this association's ability to provide ample metabolites to its symbionts and sustain high rates of carbon fixation and growth.
