Microbial Colonization of Earth's Subsurface: A Thermodynamically Consistent Perspective

The nature of how anaerobic microbes have come to distribute themselves within Earth’s crust is an ecologic question that must be posed subject to the laws of thermodynamics, but a question that cannot be understood in light of thermodynamics alone. We use here the results of theory and quantitative modeling, field observations, and long-term laboratory experiments to argue that subsurface communities are composed of groups of microbes that cooperate as well as compete, and whose existence reflects a tight balance between reproduction and cell death.

The most significant functional groups colonizing the anoxic crust, classified by electron accepting process, are the methanogens, sulfate reducers, and ferric iron reducers. An anaerobe can harvest the energy it needs to live and reproduce only to the extent that energy available to it in the environment exceeds the cell’s internal levels. When methanogens transfer or dismutate electrons, they capture little energy, so as to preserve a thermodynamic drive for their catabolic reaction. In this way, they maximize their environmental range, but grow slowly. Sulfate reducers adopt a different strategy, striving to capture energy quickly and grow rapidly. Iron reduction consumes acid, so the energy available to iron reducers varies sharply with pH. The iron reducers can grow rapidly under acidic conditions, but an alkaline environment may leave them insufficient energy to live.

Methane producers are vulnerable to exclusion in the subsurface, as is broadly appreciated, but not because of energetic limitations. Instead, the methanogens require abundant energy substrates in order to reproduce quickly enough to replace cells as they die. Sulfate reducers and iron reducers, instead of working to exclude each other by competing for limited energy sources, as is commonly believed, thrive in mutualistic communities. The three functional groups by necessity compete in their environments for limited sources of energy, but the manner in which the groups have come to colonize the subsurface is richer and more nuanced than can be explained by competition alone.