Abstract:
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
(H2), to conserve energy and fix carbon independently of photosynthesis. In
this study, we investigated whether atmospheric H2 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 hydrationdesiccation
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
H2 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 H2 oxidation was also greatly stimulated by hydration
at these sites. Together, these findings highlight that H2 is an important, hithertooverlooked
energy source supporting bacterial communities in desert soils. Contrary
to our previous hypotheses, however, H2 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 photosynthesis. In this work, we reveal that atmospheric hydrogen serves as a major previously overlooked
energy source for a large proportion of desert bacteria. We show that both chemoheterotrophic
and photoautotrophic bacteria have the potential to oxidize hydrogen across
deserts sampled across four continents. Whereas hydrogen oxidation was slow in native
dry deserts, it increased by three orders of magnitude together with photosynthesis following
hydration. This study revealed that continual harvesting of atmospheric energy
sources may be a major way that desert communities adapt to long periods of water
and energy deprivation, with significant ecological and biogeochemical ramifications.
