Frequency of change determines effectiveness of microbial response strategies in sulfidic stream microbiomes

Abstract

Nature challenges microbes with change at different frequencies and demands an effective response for survival. Here, we used controlled laboratory experiments to investigate the ecological success of different response strategies, such as post-translational modification, transcriptional regulation, and specialized versus adaptable metabolisms. For this, we inoculated replicated chemostats with an enrichment culture obtained from sulfidic stream microbiomes 16 weeks prior. The chemostats were submitted to alternatingly oxic and anoxic conditions at three frequencies, with periods of 1 day, 4 days and 16 days. The microbial response was recorded with 16S rRNA gene amplicon sequencing, shotgun metagenomics, transcriptomics and proteomics. Metagenomics resolved 26 nearly complete genomes of bacterial populations, mainly affiliated with Proteobacteria and Bacteroidetes. Almost all these populations maintained a steady growth rate under both redox conditions at all three frequencies of change. Apparently, oscillating oxic/anoxic conditions selected for generalistic species, rather than species specializing in only a single condition. Rapid (1-day) dynamics yielded more stochasticity, both in community dynamics and gene expression, indicating that bet-hedging might be an effective coping strategy for relatively rapid environmental change. Codon-usage bias, previously associated with copiotrophic and oligotrophic lifestyles, was found to be a powerful predictor of ecological success at different frequencies, with copiotrophs and oligotrophs more successful at a rapid and a slow pace of change, respectively, independent of growth rate.