Syntrophic propionate-oxidizing bacteria in methanogenic systems

Abstract

The mutual nutritional cooperation underpinning syntrophic propionate degradation provides a scant amount of energy for the microorganisms involved, so propionate degradation often acts as a bottleneck in methanogenic systems. Understanding the ecology, physiology, and metabolic capacities of syntrophic propionate-oxidizing bacteria is of interest in both engineered and natural ecosystems, as it offers prospects to guide further development of technologies for biogas production and biomass-derived chemicals, and is important in forecasting contributions by biogenic methane emissions to climate change. Syntrophic propionate-oxidizing bacteria are distributed across different phyla. They can exhibit broad metabolic capabilities in addition to syntrophy (e.g. fermentative, sulfidogenic, and acetogenic metabolism) and demonstrate variations in interplay with cooperating partners, indicating nuances in their syntrophic lifestyle. In this review, we discuss distinctions in gene repertoire and organization for the methylmalonyl-CoA pathway, hydrogenases and formate dehydrogenases, and emerging facets of (formate/hydrogen/direct) electron transfer mechanisms. We also use information from cultivations, thermodynamic calculations, and omic analyses as the basis for identifying environmental conditions governing propionate oxidation in various ecosystems. Overall, this review improves basic and applied understanding of syntrophic propionate-oxidizing bacteria and highlights knowledge gaps, hopefully encouraging future research and engineering on propionate metabolism in biotechnological processes.

Microbial community development during syngas methanation in a trickle bed reactor with various nutrient sources

“…However, in contrast, genus W27, within family Cloacimonadaceae, was highly abundant in period 2A and not detected in the nutrient medium. As mentioned earlier, members within this taxonomic group are suggested to be involved in propionate degradation (Westerholm et al 2021). However, it is difficult to predict the role of genus W27 in the present study, as it was highly abundant in period 2A after VFA had been degraded and disappeared in phase 2B.…”

“…Organic acids were degraded in the second period of operation in this study (period 2), which allowed a higher syngas load and initially resulted in slightly increased methane productivity. Degradation of propionate proceeds via syntrophic collaboration and results in formation of acetate and hydrogen, which if present in high levels can block further degradation (Westerholm et al 2021). Hydrogen is used by methanogens, but acetate can be converted via acetoclastic methanogens or via SAO (Westerholm et al 2021;Sancho Navarro et al 2016).…”

“…Degradation of propionate proceeds via syntrophic collaboration and results in formation of acetate and hydrogen, which if present in high levels can block further degradation (Westerholm et al 2021). Hydrogen is used by methanogens, but acetate can be converted via acetoclastic methanogens or via SAO (Westerholm et al 2021;Sancho Navarro et al 2016). No acetoclastic methanogens were detected in period 1, which might explain why acetate accumulated, although accumulation could also have been caused by decreased hydrogenotrophic methanogenic activity, causing problems for acetate degradation via SAO.…”

Effect of magnetite addition on transcriptional profiles of syntrophic Bacteria and Archaea during anaerobic digestion of propionate in wastewater sludge

“…Syntrophic propionate oxidation is carried out by rather specialized microorganisms (Li et al, 2012). To date, only 10 syntrophic propionate-oxidizing bacteria (SPOB) have been described in pure cultures or syntrophic co-cultures, which affiliate with the genera Desulfofundulus and Pelotomaculum (Firmicutes) and Syntrophobacter, Syntrophobacterium and Smithella (Desulfobacterota) (Westerholm et al, 2022). Almost all were isolated from anaerobic digesters (Boone and Bryant, 1980;Wallrabenstein et al, 1995;Nilsen et al, 1996;Harmsen et al, 1998;Liu et al, 1999;Imachi et al, 2002, Imachi et al, 2007Plugge et al, 2002;Chen et al, 2005;de Bok et al, 2005).…”

Modeling a propionate‐oxidizing syntrophic coculture using thermodynamic principles

“…The main drawback of ADM1 is the requirement of numerous parameters (i.e., biomass yields and growth rates; Astals et al, 2013), which are poorly described in the literature for some microorganisms such as syntrophic bacteria (Hattori, 2008; Westerholm et al, 2016; Westerholm et al, 2021). Some of these parameters are commonly calibrated using experimental data (i.e., inhibition and Monod half‐saturation constants), which triggers risks of model overfitting (Patón & Rodríguez, 2019a).…”