Breathing air to save energy – new insights into the ecophysiological role of high‐affinity [NiFe]‐hydrogenase in Streptomyces avermitilis

The Streptomyces avermitilis genome encodes a putative high‐affinity [NiFe]‐hydrogenase conferring the ability to oxidize tropospheric H(2) in mature spores. Here, we used a combination of transcriptomic and mutagenesis approaches to shed light on the potential ecophysiological role of the enzyme. First, S. avermitilis was either exposed to low or hydrogenase‐saturating levels of H(2) to investigate the impact of H(2) on spore transcriptome. In total, 1293 genes were differentially expressed, with 1127 and 166 showing lower and higher expression under elevated H(2) concentration, respectively. High H(2) exposure lowered the expression of the Sec protein secretion pathway and ATP‐binding cassette‐transporters, with increased expression of genes encoding proteins directing carbon metabolism toward sugar anabolism and lower expression of NADH dehydrogenase in the respiratory chain. Overall, the expression of relA responsible for the synthesis of the pleiotropic alarmone ppGpp decreased upon elevated H(2) exposure, which likely explained the reduced expression of antibiotic synthesis and stress response genes. Finally, deletion of hhySL genes resulted in a loss of H(2) uptake activity and a dramatic loss of viability in spores. We propose that H(2) is restricted to support the seed bank of Streptomyces under a unique survival–mixotrophic energy mode and discuss important ecological implications of this finding.