Hydrogen-Oxidizing Bacteria Are Abundant in Desert Soils and Strongly Stimulated by Hydration

• Published in: mSystems
• Main Authors: Jordaan, Karen, Lappan, Rachael, Dong, Xiyang, Aitkenhead, Ian J., Bay, Sean K., Chiri, Eleonora, Wieler, Nimrod, Meredith, Laura K., Cowan, Don A., Chown, Steven L., Greening, Chris
• Format: Text
• Language: English
• Published: American Society for Microbiology 2020
• Subjects: Research Article; Antarctic; Antarc*
• Online Access: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7677003/; http://www.ncbi.nlm.nih.gov/pubmed/33203691; https://doi.org/10.1128/mSystems.01131-20

How the diverse bacterial communities inhabiting desert soils maintain energy and carbon needs is much debated. Traditionally, most bacteria are thought to persist by using organic carbon synthesized by photoautotrophs following transient hydration events. Recent studies focused on Antarctic desert soils have revealed, however, that some bacteria use atmospheric trace gases, such as hydrogen (H(2)), to conserve energy and fix carbon independently of photosynthesis. In this study, we investigated whether atmospheric H(2) oxidation occurs in four nonpolar desert soils and compared this process to photosynthesis. To do so, we first profiled the distribution, expression, and activities of hydrogenases and photosystems in surface soils collected from the South Australian desert over a simulated hydration-desiccation cycle. Hydrogenase-encoding sequences were abundant in the metagenomes and metatranscriptomes and were detected in actinobacterial, acidobacterial, and cyanobacterial metagenome-assembled genomes. Native dry soil samples mediated H(2) oxidation, but rates increased 950-fold following wetting. Oxygenic and anoxygenic phototrophs were also detected in the community but at lower abundances. Hydration significantly stimulated rates of photosynthetic carbon fixation and, to a lesser extent, dark carbon assimilation. Hydrogenase genes were also widespread in samples from three other climatically distinct deserts, the Namib, Gobi, and Mojave, and atmospheric H(2) oxidation was also greatly stimulated by hydration at these sites. Together, these findings highlight that H(2) is an important, hitherto-overlooked energy source supporting bacterial communities in desert soils. Contrary to our previous hypotheses, however, H(2) oxidation occurs simultaneously rather than alternately with photosynthesis in such ecosystems and may even be mediated by some photoautotrophs. IMPORTANCE Desert ecosystems, spanning a third of the earth’s surface, harbor remarkably diverse microbial life despite having a low potential for ...