Acetylenotrophy: a hidden but ubiquitous microbial metabolism?

Abstract

Acetylene (IUPAC name: ethyne) is a colorless, gaseous hydrocarbon, composed of two triple bonded carbon atoms attached to hydrogens (C2H2). When microbiologists and biogeochemists think of acetylene, they immediately think of its use as an inhibitory compound of certain microbial processes and a tracer for nitrogen fixation. However, what is less widely known is that anaerobic and aerobic microorganisms can degrade acetylene, using it as a sole carbon and energy source and providing the basis of a microbial food web. Here, we review what is known about acetylene degrading organisms and introduce the term 'acetylenotrophs' to refer to the microorganisms that carry out this metabolic pathway. In addition, we review the known environmental sources of acetylene and postulate the presence of an hidden acetylene cycle. The abundance of bacteria capable of using acetylene and other alkynes as an energy and carbon source suggests that there are energy cycles present in the environment that are driven by acetylene and alkyne production and consumption that are isolated from atmospheric exchange. Acetylenotrophs may have developed to leverage the relatively high concentrations of acetylene in the pre-Cambrian atmosphere, evolving later to survive in specialized niches where acetylene and other alkynes were produced.

Figure 1.

Pathways of acetylene transformation via acetylene fermentation (left process, red) and N₂ase (right process, blue). Genes in the acetylene fermentation pathway include acetylene hydratase (AH), ALDH, ADH, phosphate acetyltransferase (PTA) and acetate kinase (AK). Modified from (Caspi et al.; Akob et al.2017).

Figure 2.

Acetylenotrophy-driven microbial food web. Sources of acetylene include known and hypothetical (green circles) sources.

Figure 3.

Syntenic map of acetylene hydratase (ahy) and flanking genes in Pelobacter sp. strain SFB93 and P. acetylenicus DSM3246 and DSM3247. Strain SFB93 contains two ahy genes in two regions, separated by ∼18,000 bp. Reprinted from (Akob et al.2017).

Figure 4.

Neighbor-joining tree showing the relationship between amino acid sequences for known and select putative AH and dehydrogenase proteins. All proteins shown contain both a molybdopterin-binding domain (conserved protein domain family cd00368) and a molybdopterin-binding C-terminal (cd02775). Putative AH containing a molybdopterin-binding acetylene hydratase (cd02759) and a molybdopterin-binding acetylene hydratase C-terminal (cd02781) are indicated with green squares and known AH are indicated by red triangles. The phylogenetic affiliation of the organisms is indicated by color. The tree was constructed by downloading amino acid (aa) sequences that matched a key-word search of 'acetylene hydratase' in the NCBI GenBank database. Additional dehydrogenase sequences were included for reference. Sequences were aligned in Geneious v. 9.1.8 (Kearse et al.2012) using the ClustalW aligner then trimmed to a final length of 980 aa to compare overlapping regions of sequence. The tree was constructed using the Geneious Tree Builder with neighbor-joining methods and Jukes-Cantor distance model.

Figure 5.

Acrylic acid and DMS are decomposition products of DMSP. Acrylic acid is hypothesized to be microbially oxidized to acetylene thereby potentially fueling a hidden acetylene cycle. The reaction from acrylic acid to acetylene yields a free energy of ΔG_reaction = −623.2 + 209.9 - (−291.5) = −121.8 kJ mol⁻¹.