Anaerobic Biohydrogenation of Isoprene by Acetobacterium wieringae Strain Y

Abstract

ABSTRACT Isoprene is a ubiquitously distributed, biogenic, and climate-active organic compound. Microbial isoprene degradation in oxic environments is fairly well understood; however, studies exploring anaerobic isoprene metabolism remain scarce, with no isolates for study available. Here, we obtained an acetogenic isolate, designated Acetobacterium wieringae strain Y, which hydrogenated isoprene to a mixture of methyl-1-butenes at an overall rate of 288.8 ± 20.9 μM day−1 with concomitant acetate production at a rate of 478.4 ± 5.6 μM day−1. Physiological characterization demonstrated that isoprene was not utilized in a respiratory process; rather, isoprene promoted acetogenesis kinetically. Bioinformatic analysis and proteomics experiments revealed the expression of candidate ene-reductases responsible for isoprene biohydrogenation. Notably, the addition of isoprene to strain Y cultures stimulated the expression of proteins associated with the Wood-Ljungdahl pathway, indicating unresolved impacts of isoprene on carbon cycling and microbial ecology in anoxic environments (e.g., promoting CO2 plus H2 reductive acetogenesis while inhibiting methanogenesis). Our new findings advance understanding of microbial transformation of isoprene under anoxic conditions and suggest that anoxic environments are isoprene sinks. IMPORTANCE Isoprene is the most abundant, biologically generated, volatile organic compound on Earth, with estimated emissions in the same magnitude as methane. Nonetheless, a comprehensive knowledge of isoprene turnover in the environment is lacking, impacting global isoprene flux models and our understanding of the environmental fate and longevity of isoprene. A critical knowledge gap that has remained largely unexplored until recently is the microbiology and associated molecular mechanisms involved in the anaerobic biotransformation of isoprene. By integrating culture-dependent approaches with omics techniques, we isolated an acetogen, Acetobacterium wieringae strain Y, capable of anaerobic biohydrogenation of isoprene. We obtained the complete genome of strain Y, and proteomic experiments identified candidate ene-reductases for catalyzing the asymmetric reduction of the electronically activated carbon-carbon double bond of isoprene. We also demonstrated that isoprene biohydrogenation stimulates the expression of Wood-Ljungdahl pathway enzymes. This study emphasizes the ecological roles of specialized Acetobacterium on the natural cycling of isoprene in anoxic environments and the potential effects of isoprene biohydrogenation on acetogens and methanogens, which have implications for global climate change and bioenergy production.

Keywords

• Acetobacterium
• biohydrogenation
• biotransformation
• ene-reductase
• isoprene