The Potential for Redox-Active Metabolites To Enhance or Unlock Anaerobic Survival Metabolisms in Aerobes

Abstract

Classifying microorganisms as “obligate” aerobes has colloquially implied death without air, leading to the erroneous assumption that, without oxygen, they are unable to survive. However, over the past few decades, more than a few obligate aerobes have been found to possess anaerobic energy conservation strategies that sustain metabolic activity in the absence of growth or at very low growth rates. Similarly, studies emphasizing the aerobic prowess of certain facultative aerobes have sometimes led to underrecognition of their anaerobic capabilities. Yet an inescapable consequence of the affinity both obligate and facultative aerobes have for oxygen is that the metabolism of these organisms may drive this substrate to scarcity, making anoxic survival an essential skill. To illustrate this, we highlight the importance of anaerobic survival strategies for Pseudomonas aeruginosa and Streptomyces coelicolor, representative facultative and obligate aerobes, respectively. Included among these strategies, we describe a role for redox-active secondary metabolites (RAMs), such as phenazines made by P. aeruginosa, in enhancing substrate-level phosphorylation. Importantly, RAMs are made by diverse bacteria, often during stationary phase in the absence of oxygen, and can sustain anoxic survival. We present a hypothesis for how RAMs may enhance or even unlock energy conservation pathways that facilitate the anaerobic survival of both RAM producers and nonproducers.

A Genome-Scale Insight into the Effect of Shear Stress During the Fed-Batch Production of Clavulanic Acid by Streptomyces Clavuligerus

“…Organic acid secretion in streptomycetes ( Figure 2 b–g) is related to an imbalance in carbon fluxes between glycolysis and the TCA cycle under carbon source abundance, also referred to as overflow metabolism [ 45 , 46 ]. Acid secretion can be also related with the activation of secondary metabolism in some Streptomyces species like S. coelicolor and S. clavuligerus [ 10 , 47 ].…”

Long-read metagenomics of soil communities reveals phylum-specific secondary metabolite dynamics

“…1 e ). We also found 17 phenazines in our dataset, some of which may have functions in redox balance during anoxia 39 , most of which belonged to cyanobacteria.…”

“…In addition to antagonism, night-time expression of BGC products can facilitate electron and nutrient transport. Redox-active secondary metabolites are known to be produced by microbes under anoxic conditions 39 . For example, Pseudomonas aeruginosa enhances substrate-level phosphorylation during anoxia through the production of phenazines that facilitate electron transport 47 .…”

Spatially resolved analysis of Pseudomonas aeruginosa biofilm proteomes measured by laser ablation sample transfer

“…The soluble transhydrogenase protein (SthA) also displayed a twofold higher abundance in the anoxic region potentially linking the conversion of anabolic and catabolic electrons. The exchange of redox active metabolites could enable respiration at a distance using small molecules like phenazines, although proteins associated with these processes were not identified [54,55].…”