Search for the role of a Huc-type [NiFe]-hydrogenase of the soil thermophile Parageobacillus thermoglucosidasius

Margarida M. Santana^1,2*Jose A. Delgado³Ana Paula Rosa⁴Cristina Cruz¹Juan M Gonzalez^5*

• ¹Centre for Ecology, Evolution and Environmental Changes (cE3c) & Global Change and Sustainability Institute (CHANGE), Faculty of Sciences, University of Lisbon, Lisbon, Portugal
• ²School of Agriculture, Santarem Polytechnic University, Santarem, Portugal
• ³University of Loyola, Dos Hermanas, Sevilla, Spain
• ⁴Centre for Ecology, Evolution and Environmental Changes (cE3c) & Global Change and Sustainability Institute (CHANGE), Faculty of Sciences, University of Lisbon,, Lisbon, Portugal
• ⁵Institute of Natural Resources and Agrobiology of Seville, Spanish National Research Council (CSIC), Seville, Spain

Previously published data showed the ubiquity of thermophilic bacteria in upper soil layers and their potential significant role in biogeochemical cycles. The processes for the maintenance of cell viability by these thermophiles in soils, including cool temperate soils, are largely unknown. We used culturing systems to mimic and analyze usual environmental growth-limiting conditions and near-zero growth rates, namely those imposed by carbon availability, and common in soils. Our goal was to comprehend how a thermophilic bacterium of the Bacillota Phylum, Parageobacillus thermoglucosidasius 23.6, persists and maintains its viability in upper soils. Comparative transcriptomic analysis of P. thermoglucosidasius 23.6 at optimum growth rate (2.2 h-1), slow growth (0.025 h-1 and 0.002 h-1) and near-zero growth rate (0.0002 h-1) revealed the overexpression of [NiFe]-hydrogenase-encoding genes, specifically of those encoding a putative Huc-type high affinity [NiFe]-hydrogenase, under growth limiting conditions. High affinity [NiFe]-hydrogenases were previously shown to be enzymes yielding energy during carbon starvation and to have a major role in the oxidation of tropospheric H2 in soil ecosystems; their activity has been proposed as a major sink for global atmospheric H2. The presence and expression of these high affinity [NiFe]-hydrogenase-encoding genes are suggested to represent a widespread strategy of terrestrial bacteria, specifically of soil thermophiles, to stay energized among resource variability or limitation, which could be considered a critical mechanism to maintain viability under growth limiting conditions to ensure long-term persistence in soils.