Enrichment of Marinobacter sp. and Halophilic Homoacetogens at the Biocathode of Microbial Electrosynthesis System Inoculated With Red Sea Brine Pool

Homoacetogens are efficient CO2 fixing bacteria using H2 as electron donor to produce acetate. These organisms can be enriched at the biocathode of microbial electrosynthesis (MES) for electricity-driven CO2 reduction to acetate. Studies exploring homoacetogens in MES are mainly conducted using pure...

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Main Authors: Manal F. Alqahtani, Suman Bajracharya, Krishna P. Katuri, Muhammad Ali, Ala’a Ragab, Grégoire Michoud, Daniele Daffonchio, Pascal E. Saikaly
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-11-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.02563/full
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language English
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author Manal F. Alqahtani
Suman Bajracharya
Krishna P. Katuri
Muhammad Ali
Ala’a Ragab
Grégoire Michoud
Daniele Daffonchio
Pascal E. Saikaly
spellingShingle Manal F. Alqahtani
Suman Bajracharya
Krishna P. Katuri
Muhammad Ali
Ala’a Ragab
Grégoire Michoud
Daniele Daffonchio
Pascal E. Saikaly
Enrichment of Marinobacter sp. and Halophilic Homoacetogens at the Biocathode of Microbial Electrosynthesis System Inoculated With Red Sea Brine Pool
Frontiers in Microbiology
Red Sea brine pool
microbial electrosynthesis
metagenome-assembled genome
marinobacter
halophilic homoacetogens
author_facet Manal F. Alqahtani
Suman Bajracharya
Krishna P. Katuri
Muhammad Ali
Ala’a Ragab
Grégoire Michoud
Daniele Daffonchio
Pascal E. Saikaly
author_sort Manal F. Alqahtani
title Enrichment of Marinobacter sp. and Halophilic Homoacetogens at the Biocathode of Microbial Electrosynthesis System Inoculated With Red Sea Brine Pool
title_short Enrichment of Marinobacter sp. and Halophilic Homoacetogens at the Biocathode of Microbial Electrosynthesis System Inoculated With Red Sea Brine Pool
title_full Enrichment of Marinobacter sp. and Halophilic Homoacetogens at the Biocathode of Microbial Electrosynthesis System Inoculated With Red Sea Brine Pool
title_fullStr Enrichment of Marinobacter sp. and Halophilic Homoacetogens at the Biocathode of Microbial Electrosynthesis System Inoculated With Red Sea Brine Pool
title_full_unstemmed Enrichment of Marinobacter sp. and Halophilic Homoacetogens at the Biocathode of Microbial Electrosynthesis System Inoculated With Red Sea Brine Pool
title_sort enrichment of marinobacter sp. and halophilic homoacetogens at the biocathode of microbial electrosynthesis system inoculated with red sea brine pool
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2019-11-01
description Homoacetogens are efficient CO2 fixing bacteria using H2 as electron donor to produce acetate. These organisms can be enriched at the biocathode of microbial electrosynthesis (MES) for electricity-driven CO2 reduction to acetate. Studies exploring homoacetogens in MES are mainly conducted using pure or mix-culture anaerobic inocula from samples with standard environmental conditions. Extreme marine environments host unique microbial communities including homoacetogens that may have unique capabilities due to their adaptation to harsh environmental conditions. Anaerobic deep-sea brine pools are hypersaline and metalliferous environments and homoacetogens can be expected to live in these environments due to their remarkable metabolic flexibility and energy-efficient biosynthesis. However, brine pools have never been explored as inocula for the enrichment of homacetogens in MES. Here we used the saline water from a Red Sea brine pool as inoculum for the enrichment of halophilic homoacetogens at the biocathode (−1 V vs. Ag/AgCl) of MES. Volatile fatty acids, especially acetate, along with hydrogen gas were produced in MES systems operated at 25 and 10% salinity. Acetate concentration increased when MES was operated at a lower salinity ∼3.5%, representing typical seawater salinity. Amplicon sequencing and genome-centric metagenomics of matured cathodic biofilm showed dominance of the genus Marinobacter and phylum Firmicutes at all tested salinities. Seventeen high-quality draft metagenome-assembled genomes (MAGs) were extracted from the biocathode samples. The recovered MAGs accounted for 87 ± 4% of the quality filtered sequence reads. Genome analysis of the MAGs suggested CO2 fixation via Wood–Ljundahl pathway by members of the phylum Firmicutes and the fixed CO2 was possibly utilized by Marinobacter sp. for growth by consuming O2 escaping from the anode to the cathode for respiration. The enrichment of Marinobacter sp. with homoacetogens was only possible because of the specific cathodic environment in MES. These findings suggest that in organic carbon-limited saline environments, Marinobacter spp. can live in consortia with CO2 fixing bacteria such as homoacetogens, which can provide them with fixed carbon as a source of carbon and energy.
topic Red Sea brine pool
microbial electrosynthesis
metagenome-assembled genome
marinobacter
halophilic homoacetogens
url https://www.frontiersin.org/article/10.3389/fmicb.2019.02563/full
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spelling doaj-c2661e080dbc40f4b28c056739a5627e2020-11-25T02:03:30ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-11-011010.3389/fmicb.2019.02563486066Enrichment of Marinobacter sp. and Halophilic Homoacetogens at the Biocathode of Microbial Electrosynthesis System Inoculated With Red Sea Brine PoolManal F. Alqahtani0Suman Bajracharya1Krishna P. Katuri2Muhammad Ali3Ala’a Ragab4Grégoire Michoud5Daniele Daffonchio6Pascal E. Saikaly7King Abdullah University of Science and Technology, Water Desalination and Reuse Center, Biological and Environmental Science and Engineering Division, Thuwal, Saudi ArabiaKing Abdullah University of Science and Technology, Water Desalination and Reuse Center, Biological and Environmental Science and Engineering Division, Thuwal, Saudi ArabiaKing Abdullah University of Science and Technology, Water Desalination and Reuse Center, Biological and Environmental Science and Engineering Division, Thuwal, Saudi ArabiaKing Abdullah University of Science and Technology, Water Desalination and Reuse Center, Biological and Environmental Science and Engineering Division, Thuwal, Saudi ArabiaKing Abdullah University of Science and Technology, Water Desalination and Reuse Center, Biological and Environmental Science and Engineering Division, Thuwal, Saudi ArabiaKing Abdullah University of Science and Technology, Red Sea Research Center, Biological and Environmental Science and Engineering Division, Thuwal, Saudi ArabiaKing Abdullah University of Science and Technology, Red Sea Research Center, Biological and Environmental Science and Engineering Division, Thuwal, Saudi ArabiaKing Abdullah University of Science and Technology, Water Desalination and Reuse Center, Biological and Environmental Science and Engineering Division, Thuwal, Saudi ArabiaHomoacetogens are efficient CO2 fixing bacteria using H2 as electron donor to produce acetate. These organisms can be enriched at the biocathode of microbial electrosynthesis (MES) for electricity-driven CO2 reduction to acetate. Studies exploring homoacetogens in MES are mainly conducted using pure or mix-culture anaerobic inocula from samples with standard environmental conditions. Extreme marine environments host unique microbial communities including homoacetogens that may have unique capabilities due to their adaptation to harsh environmental conditions. Anaerobic deep-sea brine pools are hypersaline and metalliferous environments and homoacetogens can be expected to live in these environments due to their remarkable metabolic flexibility and energy-efficient biosynthesis. However, brine pools have never been explored as inocula for the enrichment of homacetogens in MES. Here we used the saline water from a Red Sea brine pool as inoculum for the enrichment of halophilic homoacetogens at the biocathode (−1 V vs. Ag/AgCl) of MES. Volatile fatty acids, especially acetate, along with hydrogen gas were produced in MES systems operated at 25 and 10% salinity. Acetate concentration increased when MES was operated at a lower salinity ∼3.5%, representing typical seawater salinity. Amplicon sequencing and genome-centric metagenomics of matured cathodic biofilm showed dominance of the genus Marinobacter and phylum Firmicutes at all tested salinities. Seventeen high-quality draft metagenome-assembled genomes (MAGs) were extracted from the biocathode samples. The recovered MAGs accounted for 87 ± 4% of the quality filtered sequence reads. Genome analysis of the MAGs suggested CO2 fixation via Wood–Ljundahl pathway by members of the phylum Firmicutes and the fixed CO2 was possibly utilized by Marinobacter sp. for growth by consuming O2 escaping from the anode to the cathode for respiration. The enrichment of Marinobacter sp. with homoacetogens was only possible because of the specific cathodic environment in MES. These findings suggest that in organic carbon-limited saline environments, Marinobacter spp. can live in consortia with CO2 fixing bacteria such as homoacetogens, which can provide them with fixed carbon as a source of carbon and energy.https://www.frontiersin.org/article/10.3389/fmicb.2019.02563/fullRed Sea brine poolmicrobial electrosynthesismetagenome-assembled genomemarinobacterhalophilic homoacetogens