Cryptic roles of tetrathionate in the sulfur cycle of marine sediments: microbial drivers and indicators

<p>To explore the potential role of tetrathionate in the sedimentary sulfur cycle, population ecology of microorganisms capable of metabolizing this polythionate was revealed at 15–30&thinsp;cm resolution along two, <span class="inline-formula">∼3</span>&thinsp;m...

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Main Authors: S. Mandal, S. Bhattacharya, C. Roy, M. J. Rameez, J. Sarkar, T. Mapder, S. Fernandes, A. Peketi, A. Mazumdar, W. Ghosh
Format: Article
Language:English
Published: Copernicus Publications 2020-09-01
Series:Biogeosciences
Online Access:https://bg.copernicus.org/articles/17/4611/2020/bg-17-4611-2020.pdf
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author S. Mandal
S. Bhattacharya
C. Roy
M. J. Rameez
J. Sarkar
T. Mapder
T. Mapder
S. Fernandes
A. Peketi
A. Mazumdar
W. Ghosh
author_facet S. Mandal
S. Bhattacharya
C. Roy
M. J. Rameez
J. Sarkar
T. Mapder
T. Mapder
S. Fernandes
A. Peketi
A. Mazumdar
W. Ghosh
author_sort S. Mandal
collection DOAJ
description <p>To explore the potential role of tetrathionate in the sedimentary sulfur cycle, population ecology of microorganisms capable of metabolizing this polythionate was revealed at 15–30&thinsp;cm resolution along two, <span class="inline-formula">∼3</span>&thinsp;m long, cores collected from 530 and 580&thinsp;m below the sea level, off India's west coast, within the oxygen minimum zone (OMZ) of the Arabian Sea. Metagenome analysis along the cores revealed widespread occurrence of genes involved in the formation, oxidation, and reduction of tetrathionate; high diversity and relative abundance were also detected for bacteria that are known to render these metabolisms in vitro. Results of slurry culture of the sediment samples in thiosulfate- or tetrathionate-containing microbial growth media, data obtained via pure-culture isolation, and finally metatranscriptome analyses corroborated the in situ functionality of the tetrathionate-forming, tetrathionate-oxidizing, and tetrathionate-reducing microorganisms. Ion chromatography of pore waters revealed the presence of up to 11.1&thinsp;<span class="inline-formula">µ</span>M thiosulfate in the two cores, whereas tetrathionate remained undetected in spectroscopic assay based on its reaction with cyanide. While thiosulfate oxidation by chemolithotrophic bacteria prevalent in situ is the apparent source of tetrathionate in this ecosystem, high biochemical and geochemical reactivity of this polythionate could be instrumental in its cryptic status in the sulfur cycle. Potential abiotic origin of tetrathionate in the sediment horizon explored could neither be ruled out nor confirmed from the geochemical information available. On the other hand, tetrathionate potentially present in the system can be either oxidized to sulfate or reduced back to thiosulfate/sulfide via chemolithotrophic oxidation and respiration by native bacterial populations, respectively. Up to 2.01&thinsp;mM sulfide present in the sediment cores may also reduce tetrathionate abiotically to thiosulfate and elemental sulfur. However, in the absence of measured data for <span class="inline-formula">O<sub>2</sub></span> or other oxyanions having possibilities of serving as electron acceptors, the biogeochemical modalities of the oxidative half of the tetrathionate cycle remained unresolved.</p>
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spelling doaj.art-fa93a69f5d884118b58f72602d2a2c622022-12-22T00:45:00ZengCopernicus PublicationsBiogeosciences1726-41701726-41892020-09-01174611463110.5194/bg-17-4611-2020Cryptic roles of tetrathionate in the sulfur cycle of marine sediments: microbial drivers and indicatorsS. Mandal0S. Bhattacharya1C. Roy2M. J. Rameez3J. Sarkar4T. Mapder5T. Mapder6S. Fernandes7A. Peketi8A. Mazumdar9W. Ghosh10Department of Microbiology, Bose Institute, P-1/12 CIT Scheme VIIM, Kolkata 700054, IndiaDepartment of Microbiology, Bose Institute, P-1/12 CIT Scheme VIIM, Kolkata 700054, IndiaDepartment of Microbiology, Bose Institute, P-1/12 CIT Scheme VIIM, Kolkata 700054, IndiaDepartment of Microbiology, Bose Institute, P-1/12 CIT Scheme VIIM, Kolkata 700054, IndiaDepartment of Microbiology, Bose Institute, P-1/12 CIT Scheme VIIM, Kolkata 700054, IndiaARC CoE for Mathematical and Statistical Frontiers, School of Mathematical Sciences, Queensland University of Technology, Brisbane, QLD 4000, Australiapresent address: Department of Medicine, Indiana University School of Medicine, Indianapolis, IN 46202, USAGas Hydrate Research Group, Geological Oceanography, CSIR-National Institute of Oceanography, Dona Paula, Goa 403004, IndiaGas Hydrate Research Group, Geological Oceanography, CSIR-National Institute of Oceanography, Dona Paula, Goa 403004, IndiaGas Hydrate Research Group, Geological Oceanography, CSIR-National Institute of Oceanography, Dona Paula, Goa 403004, IndiaDepartment of Microbiology, Bose Institute, P-1/12 CIT Scheme VIIM, Kolkata 700054, India<p>To explore the potential role of tetrathionate in the sedimentary sulfur cycle, population ecology of microorganisms capable of metabolizing this polythionate was revealed at 15–30&thinsp;cm resolution along two, <span class="inline-formula">∼3</span>&thinsp;m long, cores collected from 530 and 580&thinsp;m below the sea level, off India's west coast, within the oxygen minimum zone (OMZ) of the Arabian Sea. Metagenome analysis along the cores revealed widespread occurrence of genes involved in the formation, oxidation, and reduction of tetrathionate; high diversity and relative abundance were also detected for bacteria that are known to render these metabolisms in vitro. Results of slurry culture of the sediment samples in thiosulfate- or tetrathionate-containing microbial growth media, data obtained via pure-culture isolation, and finally metatranscriptome analyses corroborated the in situ functionality of the tetrathionate-forming, tetrathionate-oxidizing, and tetrathionate-reducing microorganisms. Ion chromatography of pore waters revealed the presence of up to 11.1&thinsp;<span class="inline-formula">µ</span>M thiosulfate in the two cores, whereas tetrathionate remained undetected in spectroscopic assay based on its reaction with cyanide. While thiosulfate oxidation by chemolithotrophic bacteria prevalent in situ is the apparent source of tetrathionate in this ecosystem, high biochemical and geochemical reactivity of this polythionate could be instrumental in its cryptic status in the sulfur cycle. Potential abiotic origin of tetrathionate in the sediment horizon explored could neither be ruled out nor confirmed from the geochemical information available. On the other hand, tetrathionate potentially present in the system can be either oxidized to sulfate or reduced back to thiosulfate/sulfide via chemolithotrophic oxidation and respiration by native bacterial populations, respectively. Up to 2.01&thinsp;mM sulfide present in the sediment cores may also reduce tetrathionate abiotically to thiosulfate and elemental sulfur. However, in the absence of measured data for <span class="inline-formula">O<sub>2</sub></span> or other oxyanions having possibilities of serving as electron acceptors, the biogeochemical modalities of the oxidative half of the tetrathionate cycle remained unresolved.</p>https://bg.copernicus.org/articles/17/4611/2020/bg-17-4611-2020.pdf
spellingShingle S. Mandal
S. Bhattacharya
C. Roy
M. J. Rameez
J. Sarkar
T. Mapder
T. Mapder
S. Fernandes
A. Peketi
A. Mazumdar
W. Ghosh
Cryptic roles of tetrathionate in the sulfur cycle of marine sediments: microbial drivers and indicators
Biogeosciences
title Cryptic roles of tetrathionate in the sulfur cycle of marine sediments: microbial drivers and indicators
title_full Cryptic roles of tetrathionate in the sulfur cycle of marine sediments: microbial drivers and indicators
title_fullStr Cryptic roles of tetrathionate in the sulfur cycle of marine sediments: microbial drivers and indicators
title_full_unstemmed Cryptic roles of tetrathionate in the sulfur cycle of marine sediments: microbial drivers and indicators
title_short Cryptic roles of tetrathionate in the sulfur cycle of marine sediments: microbial drivers and indicators
title_sort cryptic roles of tetrathionate in the sulfur cycle of marine sediments microbial drivers and indicators
url https://bg.copernicus.org/articles/17/4611/2020/bg-17-4611-2020.pdf
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