Acetogenesis in the Energy-Starved Deep Biosphere – A Paradox?

Mark Alexander Lever

doi:10.3389/fmicb.2011.00284

Abstract

Under anoxic conditions in sediments, acetogens are often thought to be outcompeted by microorganisms performing energetically more favorable metabolic pathways, such as sulfate reduction or methanogenesis. Recent evidence from deep subseafloor sediments suggesting acetogenesis in the presence of sulfate reduction and methanogenesis has called this notion into question, however. Here I argue that acetogens can successfully coexist with sulfate reducers and methanogens for multiple reasons. These include (1) substantial energy yields from most acetogenesis reactions across the wide range of conditions encountered in the subseafloor, (2) wide substrate spectra that enable niche differentiation by use of different substrates and/or pooling of energy from a broad range of energy substrates, (3) reduced energetic cost of biosynthesis among acetogens due to use of the reductive acetyl CoA pathway for both energy production and biosynthesis coupled with the ability to use many organic precursors to produce the key intermediate acetyl CoA. This leads to the general conclusion that, beside Gibbs free energy yields, variables such as metabolic strategy and energetic cost of biosynthesis need to be taken into account to understand microbial survival in the energy-depleted deep biosphere.

Highlights

Past studies on anoxic sediments have demonstrated a redox zonation among terminal organic matter remineralizing microbes in relation to electron acceptor availability (e.g., Froelich et al, 1979; Canfield et al, 1993)
The results presented far suggest that it is very difficult to predict the outcome of the complex competition between acetogens and other groups for substrates in the deep biosphere
If energy yields per substrate are the only important variable controlling microbial metabolism in energy-starved subsurface sediments, acetogenic microbes should be outcompeted by other anaerobic microbes that perform energetically more favorable pathways, such as sulfate reduction and methanogenesis

Summary

INTRODUCTION

Past studies on anoxic sediments have demonstrated a redox zonation among terminal organic matter remineralizing microbes in relation to electron acceptor availability (e.g., Froelich et al, 1979; Canfield et al, 1993). In freshwater and coastal marine sediments depletion of the most favorable oxidants often occurs shallowly owing to an excess of electron donors produced by fermentation and hydrolysis reactions (Capone and Kiene, 1988). This creates a niche for methane-producing Archaea (methanogens) and acetatesynthesizing microbes (acetogens), groups that are able to harvest energy from CO2 reduction in underlying layers (e.g., Phelps and Zeikus, 1984; Avery et al, 2002; Ferry and Lessner, 2008; Liu and Conrad, 2011). Acetogenesis in the deep biosphere the potential for substrate generalism as a successful strategy under extreme energy limitation, and (3) examine the cost of biosynthesis and potential ways by which acetogens may reduce energy expended on biosynthesis

MATERIALS AND METHODS

RESULTS AND DISCUSSION

Findings

CONCLUSION