Abstract

A novel deltaproteobacterial, mesophilic, hydrogen-oxidizing, and sulfate-reducing bacterium (strain KaireiS1) was highly enriched from an inactive chimney located in the active zone of the Kairei hydrothermal vent field (Central Indian Ridge) in the Indian Ocean. Based on 16S rRNA gene analyses, strain KaireiS1 is the currently only cultured representative of a cluster of uncultured Deltaproteobacteria, positioned within the Desulfobulbaceae family, between the Desulfobulbus genus and the “Cable Bacteria.” A facultative autotrophic lifestyle of KaireiS1 is indicated by its growth in the absence of organic compounds, measurements of CO2-fixation rates, and activity measurements of carbon monoxide dehydrogenase, the key enzyme of the reductive Acetyl-CoA pathway. Apart from hydrogen, strain KaireiS1 can also use propionate, lactate, and pentadecane as electron donors. However, the highest cell numbers were reached when grown autotrophically with molecular hydrogen. Hydrogen uptake activity was found in membrane and soluble fractions of cell-free extracts and reached up to 2,981±129 nmol H2*min−1*mg−1 of partially purified protein. Commonly, autotrophic sulfate-reducing bacteria from the Deltaproteobacteria class, thriving in hydrothermal vent habitats are described as thermophiles. Given its physiological characteristics and specific isolation source, strain KaireiS1 demonstrates a previously unnoticed potential for microbial sulfate reduction by autotrophs taking place at moderate temperatures in hydrothermal vent fields.

Highlights

  • The Kairei hydrothermal field is located in the Central Indian Ridge (Gamo et al, 2001; Hashimoto et al, 2001)

  • Hydrogen-free cultures supplemented with glucose, fructose or pyruvate and fumarate, demonstrated a mix of KaireiS1 and Sunxiuqinia sp., where Sunxiuqinia accounted for 18%, 54%, and 72% of the total cell mass, respectively (Table 1)

  • Deltaproteobacterial isolates from hydrothermal vent systems that can grow autotrophically with hydrogen as electron donor are described as thermophiles with temperature optima between 50 and 61°C (Adam and Perner, 2018a and references therein)

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Summary

Introduction

The Kairei hydrothermal field is located in the Central Indian Ridge (Gamo et al, 2001; Hashimoto et al, 2001). Analyses of microbial community compositions in inactive Kairei chimneys have demonstrated the presence of members from the Desulfobulbaceae family (e.g., 2.2% Desulfobulbus spp. in the chimney sample S1; Han et al, 2018) This family currently comprises eight validated genera and two candidate genera with Desulfobulbus representing the type genus (Kuever, 2014; Junghare and Schink, 2015; Trojan et al, 2016). Candidatus Electrothrix and Candidatus Electronema form the group of Cable Bacteria that currently does not comprise axenic cultures Insights into their physiology could be gained by means of enrichment cultures, metagenomics, and incubation-experiments (Kjeldsen et al, 2019; Müller et al, 2020). Apart from organic electron donors like lactate, formate, or pyruvate, some species can use molecular hydrogen albeit only in the presence of acetate (Widdel and Pfennig, 1982; Samain et al, 1984; Lien et al, 1998; Sass et al, 2002; Suzuki et al, 2007; Sorokin et al, 2012; El Houari et al, 2017; Kharrat et al, 2017; Cross et al, 2018)

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