‘That which does not kill us only makes us stronger’: the role of carbon monoxide in thermophilic microbial consortia

Abstract

SummaryCarbon monoxide (CO), while a potent toxin, is also a key intermediate in major autotrophic pathways such as methanogenesis and acetogenesis. The ability of purple sulfur bacteria to use CO as an energy source was first described by Uffen in 1976. The prototype extremely thermophilic carboxydotroph Carboxydothermus hydrogenoformans was described in 1991. Eight bacteria and one archaeon that utilize CO have since been isolated and described from diverse geothermal environments. They derive energy from the oxidation of CO with water to form CO 2 and H2. Most of these isolates thrive with headspace CO partial pressures around 1 atm, which is grossly elevated relative to CO concentrations in geothermal effluents. To account for this, we suggest that under consortial growth conditions the carboxydotrophs occupy microniches in which biogenic CO accumulates locally to high concentrations. CO oxidizers dissipate these potentially toxic CO hot spots with the production of H2, CO2 and acetate whose subsequent oxidation fuels other thermophiles. The identification of genes related to anaerobic CO oxidation in many metagenomic databases attests to widespread distribution of carboxydotrophs. Current evidence suggests that CO-oxidizing bacteria and archaea hold a vital niche in thermophilic ecosystems.

CO metabolism, sensing, and signaling

“…Several microorganisms, including aerobic and anaerobic bacteria and anaerobic archaea, use CO as a source of carbon and energy for growth [10,11,22]. CO-metabolizing bacteria, spanning multiple phylogenetic lineages, include aerobic carboxydotrophic and carboxydovores bacteria (the latter being unable to grow in the presence of elevated CO concentrations) [9], and obligate anaerobic CO oxidizers (e.g., acetogenic bacteria, hydrogenogenic bacteria, phototrophic purple nonsulfur bacteria, and sulfate-reducing bacteria) [11].…”

“…Therefore, despite its toxicity [1,7,8], CO plays a key role in several metabolic processes and in diverse signal transduction pathways in bacteria, archaea, and eukaryotes [9][10][11].…”

“…In both prokaryotes and eukaryotes, the major molecular targets of CO are heme-proteins [12,13], which display diverse biological functions including sensing and transportation of diatomic gases, catalysis, and electron transfer [11,[13][14][15]. A number of signaling effects of CO depend on the modulation of soluble guanylate cyclase (sGC) and/or activation of mitogen-activated protein kinases (MAPKs).…”

A thermophilic, hydrogenogenic and carboxydotrophic bacterium, Calderihabitans maritimus gen. nov., sp. nov., from a marine sediment core of an undersea caldera

“…Most thermophilic carboxydotrophs oxidize CO for energy and produce molecular hydrogen or acetate (Sokolova et al, 2009). As many microbes are sensitive to CO exposure, CO-oxidation in the environment may have an important role; that is, 'scavenging' toxic CO and converting it to more commonly used substrates (Techtmann et al, 2009). Presently, whereas many isolates have been found in terrestrial hot springs, only one bacterial and three archaeal isolates of H 2 -producing (hydrogenogenic) carboxydotrophs have been found in marine environments.…”

Carboxydothermus pertinax sp. nov., a thermophilic, hydrogenogenic, Fe(III)-reducing, sulfur-reducing carboxydotrophic bacterium from an acidic hot spring

“…In such environments, thermophilic CO-oxidizing prokaryotes are assumed to play important roles as CO scavengers (Techtmann et al, 2009). Some of CO-oxidizing H 2 -producing anaerobes, such as Carboxydothermus hydrogenoformans (Svetlichny et al, 1991), are so-called 'carboxydotrophic hydrogenogens'.…”