Parameters Governing the Community Structure and Element Turnover in Kermadec Volcanic Ash and Hydrothermal Fluids as Monitored by Inorganic Electron Donor Consumption, Autotrophic CO2 Fixation and 16S Tags of the Transcriptome in Incubation Experiments

Stefanie Böhnke; Katharina Sass; Giorgio Gonnella; Alexander Diehl; Charlotte Kleint; Wolfgang Bach; Rebecca Zitoun; Andrea Koschinsky; Daniela Indenbirken; Sylvia G Sander; Stefan Kurtz; Mirjam Perner

doi:10.3389/fmicb.2019.02296

Parameters Governing the Community Structure and Element Turnover in Kermadec Volcanic Ash and Hydrothermal Fluids as Monitored by Inorganic Electron Donor Consumption, Autotrophic CO₂ Fixation and 16S Tags of the Transcriptome in Incubation Experiments

Front Microbiol. 2019 Oct 9:10:2296. doi: 10.3389/fmicb.2019.02296. eCollection 2019.

Authors

Affiliations

¹ Molecular Biology of Microbial Consortia, Institute of Plant Science and Microbiology, Universität Hamburg, Hamburg, Germany.
² Center for Bioinformatics (ZBH), Universität Hamburg, Hamburg, Germany.
³ Department of Geosciences, MARUM - Centre for Marine Environmental Sciences, University of Bremen, Bremen, Germany.
⁴ Department of Physics and Earth Sciences, Jacobs University Bremen, Bremen, Germany.
⁵ Department of Chemistry, University of Otago, Dunedin, New Zealand.
⁶ Heinrich Pette Institute, Leibniz Institute for Experimental Virology, Hamburg, Germany.

Abstract

The microbial community composition and its functionality was assessed for hydrothermal fluids and volcanic ash sediments from Haungaroa and hydrothermal fluids from the Brothers volcano in the Kermadec island arc (New Zealand). The Haungaroa volcanic ash sediments were dominated by epsilonproteobacterial Sulfurovum sp. Ratios of electron donor consumption to CO₂ fixation from respective sediment incubations indicated that sulfide oxidation appeared to fuel autotrophic CO₂ fixation, coinciding with thermodynamic estimates predicting sulfide oxidation as the major energy source in the environment. Transcript analyses with the sulfide-supplemented sediment slurries demonstrated that Sulfurovum prevailed in the experiments as well. Hence, our sediment incubations appeared to simulate environmental conditions well suggesting that sulfide oxidation catalyzed by Sulfurovum members drive biomass synthesis in the volcanic ash sediments. For the Haungaroa fluids no inorganic electron donor and responsible microorganisms could be identified that clearly stimulated autotrophic CO₂ fixation. In the Brothers hydrothermal fluids Sulfurimonas (49%) and Hydrogenovibrio/Thiomicrospira (15%) species prevailed. Respective fluid incubations exhibited highest autotrophic CO₂ fixation if supplemented with iron(II) or hydrogen. Likewise catabolic energy calculations predicted primarily iron(II) but also hydrogen oxidation as major energy sources in the natural fluids. According to transcript analyses with material from the incubation experiments Thiomicrospira/Hydrogenovibrio species dominated, outcompeting Sulfurimonas. Given that experimental conditions likely only simulated environmental conditions that cause Thiomicrospira/Hydrogenovibrio but not Sulfurimonas to thrive, it remains unclear which environmental parameters determine Sulfurimonas' dominance in the Brothers natural hydrothermal fluids.

Keywords: 16S rRNA genes; MiSeq; autotrophic CO2 fixation; microbial hydrogen oxidation; microbial hydrothermal vent communities; microbial iron oxidation; microbial sulfide oxidation.