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

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 Antarcti...

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Autores principales:	Karen Jordaan, Rachael Lappan, Xiyang Dong, Ian J. Aitkenhead, Sean K. Bay, Eleonora Chiri, Nimrod Wieler, Laura K. Meredith, Don A. Cowan, Steven L. Chown, Chris Greening
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	carbon fixation desert hydrogen hydrogenase primary production trace gas Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/f7352c5d4e574b4c9d60ec5966ece370
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spelling	oai:doaj.org-article:f7352c5d4e574b4c9d60ec5966ece3702021-12-02T18:15:47ZHydrogen-Oxidizing Bacteria Are Abundant in Desert Soils and Strongly Stimulated by Hydration10.1128/mSystems.01131-202379-5077https://doaj.org/article/f7352c5d4e574b4c9d60ec5966ece3702020-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.01131-20https://doaj.org/toc/2379-5077ABSTRACT 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 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 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, hitherto-overlooked 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. Author Video: An author video summary of this article is available.Karen JordaanRachael LappanXiyang DongIan J. AitkenheadSean K. BayEleonora ChiriNimrod WielerLaura K. MeredithDon A. CowanSteven L. ChownChris GreeningAmerican Society for Microbiologyarticlecarbon fixationdeserthydrogenhydrogenaseprimary productiontrace gasMicrobiologyQR1-502ENmSystems, Vol 5, Iss 6 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	carbon fixation desert hydrogen hydrogenase primary production trace gas Microbiology QR1-502
spellingShingle	carbon fixation desert hydrogen hydrogenase primary production trace gas Microbiology QR1-502 Karen Jordaan Rachael Lappan Xiyang Dong Ian J. Aitkenhead Sean K. Bay Eleonora Chiri Nimrod Wieler Laura K. Meredith Don A. Cowan Steven L. Chown Chris Greening Hydrogen-Oxidizing Bacteria Are Abundant in Desert Soils and Strongly Stimulated by Hydration
description	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 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 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, hitherto-overlooked 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. Author Video: An author video summary of this article is available.
format	article
author	Karen Jordaan Rachael Lappan Xiyang Dong Ian J. Aitkenhead Sean K. Bay Eleonora Chiri Nimrod Wieler Laura K. Meredith Don A. Cowan Steven L. Chown Chris Greening
author_facet	Karen Jordaan Rachael Lappan Xiyang Dong Ian J. Aitkenhead Sean K. Bay Eleonora Chiri Nimrod Wieler Laura K. Meredith Don A. Cowan Steven L. Chown Chris Greening
author_sort	Karen Jordaan
title	Hydrogen-Oxidizing Bacteria Are Abundant in Desert Soils and Strongly Stimulated by Hydration
title_short	Hydrogen-Oxidizing Bacteria Are Abundant in Desert Soils and Strongly Stimulated by Hydration
title_full	Hydrogen-Oxidizing Bacteria Are Abundant in Desert Soils and Strongly Stimulated by Hydration
title_fullStr	Hydrogen-Oxidizing Bacteria Are Abundant in Desert Soils and Strongly Stimulated by Hydration
title_full_unstemmed	Hydrogen-Oxidizing Bacteria Are Abundant in Desert Soils and Strongly Stimulated by Hydration
title_sort	hydrogen-oxidizing bacteria are abundant in desert soils and strongly stimulated by hydration
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/f7352c5d4e574b4c9d60ec5966ece370
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Hydrogen-Oxidizing Bacteria Are Abundant in Desert Soils and Strongly Stimulated by Hydration

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