Evolutionary causes and consequences of metabolic division of labour: why anaerobes do and aerobes don’t

[Display omitted] •Catabolic division of labour is prevalent in anoxic, but not in oxic environments.•Anoxic environments are oxygen depleted because of a high influx of organic matter.•Such a high flux favours evolution of shorter, incomplete pathways.•Aerobes are complete oxidizers because low flux, long pathways suffice and respiration makes more ATP at the end.•Bioreactors are high flux environments so microbes must be engineered to resist evolution to shorter pathways. Metabolic division of the labour of organic matter decomposition into several steps carried out by different types of microbes is typical for many anoxic — but not oxic environments. An explanation of this well-known pattern is proposed based on the combination of three key insights: (i) well-studied anoxic environments are high flux environments: they are only anoxic because their high organic matter influx leads to oxygen depletion; (ii) shorter, incomplete catabolic pathways provide the capacity for higher flux, but this capacity is only advantageous in high flux environments; (iii) longer, complete catabolic pathways have energetic happy ends but only with high redox potential electron acceptors. Thus, aerobic environments favour longer pathways. Bioreactors, in contrast, are high flux environments and therefore favour division of catabolic labour even if aeration keeps them aerobic; therefore, host strains and feeding strategies must be carefully engineered to resist this pull.