Enrichment of electrotrophic microorganisms from contrasting shallow-sea hydrothermal environments in bioelectrochemical reactors
IntroductionHydrothermal vents are inhabited by electrotrophic microorganisms, which are capable of oxidizing extracellular compounds, such as metals, to power their metabolisms. However, their diversity is poorly known, especially in shallow-sea hydrothermal vents where it has not been extensively...
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Frontiers Media S.A.
2025-02-01
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| author | Antoine Carissimo Victoria Comes Alenica Heussner Anne-Hélène Prime Roy E. Price Gaël Erauso Pierre-Pol Liebgott Sven Kerzenmacher Guillaume Pillot |
| author_facet | Antoine Carissimo Victoria Comes Alenica Heussner Anne-Hélène Prime Roy E. Price Gaël Erauso Pierre-Pol Liebgott Sven Kerzenmacher Guillaume Pillot |
| author_sort | Antoine Carissimo |
| collection | DOAJ |
| description | IntroductionHydrothermal vents are inhabited by electrotrophic microorganisms, which are capable of oxidizing extracellular compounds, such as metals, to power their metabolisms. However, their diversity is poorly known, especially in shallow-sea hydrothermal vents where it has not been extensively studied. Bioelectrochemical reactors can be used to investigate such electrotrophic diversity by providing an electrode as an electron donor.MethodsHere, a total of 60 different reactors were set up and inoculated with either a microbial community coming from the shallow, acidic (ca. pH 5.5) and hot (ca. 120°C) hydrothermal system of Panarea, Aeolian islands, Italy, or the shallow, alkaline (pH 11) and mild (40°C) hydrothermal system of Prony Bay, New Caledonia.ResultsWith the alkaline sample, no electrical current increase was seen in any of the 15 reactors operated for 6 days under Prony hydrothermal conditions (pH 10, 30–75°C). By contrast, a 6-fold increase on average was observed in reactors operated under the Panarea hydrothermal fluid conditions (pH 4.5–7, 75°C). A Multi-Factor Analysis revealed that the overall bioelectrochemical performances of these reactors set them apart from all the other Panarea and Prony conditions, not only due to their higher current production but also archaeal abundances (measured through qPCR). Most reactors produced organic acids (up to 2.9 mM in 6 days). Still, coulombic efficiencies indicated that this might have been due to the (electro) fermentation of traces of yeast extract in the medium rather than CO2 fixation. Finally, microbial communities were described by 16S metabarcoding and ordination methods, and potential electrotrophic taxa were identified. In Panarea reactors, higher growth was correlated with a few bacterial genera, mainly Bacillus and Pseudoalteromonas, including, for the former, at higher temperatures (55°C and 75°C). In reactors reproducing the Prony Bay hydrothermal conditions, known facultative methylotrophs, such as Sphingomonas and Methylobacterium, were dominant and appeared to consume formate (provided as carbon source) but no electrons from the cathode.ConclusionThese results provide new insights into the distribution and diversity of electrotrophs in shallow-sea hydrothermal vents and allow the identification of potential novel biocatalysts for Microbial Electrosynthesis whereby electricity and carbon dioxide are converted into value-added products. |
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| institution | Kabale University |
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| publishDate | 2025-02-01 |
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| spelling | doaj-art-2ea5465a99084623839545c41adb26772025-02-03T06:33:48ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-02-011610.3389/fmicb.2025.15396081539608Enrichment of electrotrophic microorganisms from contrasting shallow-sea hydrothermal environments in bioelectrochemical reactorsAntoine Carissimo0Victoria Comes1Alenica Heussner2Anne-Hélène Prime3Roy E. Price4Gaël Erauso5Pierre-Pol Liebgott6Sven Kerzenmacher7Guillaume Pillot8Center for Environmental Research and Sustainable Technology (UFT), University of Bremen, Bremen, GermanyCenter for Environmental Research and Sustainable Technology (UFT), University of Bremen, Bremen, GermanyCenter for Environmental Research and Sustainable Technology (UFT), University of Bremen, Bremen, GermanyAix Marseille Univ, Université de Toulon, CNRS, IRD, MIO, Marseille, FranceSchool of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY, United StatesAix Marseille Univ, Université de Toulon, CNRS, IRD, MIO, Marseille, FranceAix Marseille Univ, Université de Toulon, CNRS, IRD, MIO, Marseille, FranceCenter for Environmental Research and Sustainable Technology (UFT), University of Bremen, Bremen, GermanyCenter for Environmental Research and Sustainable Technology (UFT), University of Bremen, Bremen, GermanyIntroductionHydrothermal vents are inhabited by electrotrophic microorganisms, which are capable of oxidizing extracellular compounds, such as metals, to power their metabolisms. However, their diversity is poorly known, especially in shallow-sea hydrothermal vents where it has not been extensively studied. Bioelectrochemical reactors can be used to investigate such electrotrophic diversity by providing an electrode as an electron donor.MethodsHere, a total of 60 different reactors were set up and inoculated with either a microbial community coming from the shallow, acidic (ca. pH 5.5) and hot (ca. 120°C) hydrothermal system of Panarea, Aeolian islands, Italy, or the shallow, alkaline (pH 11) and mild (40°C) hydrothermal system of Prony Bay, New Caledonia.ResultsWith the alkaline sample, no electrical current increase was seen in any of the 15 reactors operated for 6 days under Prony hydrothermal conditions (pH 10, 30–75°C). By contrast, a 6-fold increase on average was observed in reactors operated under the Panarea hydrothermal fluid conditions (pH 4.5–7, 75°C). A Multi-Factor Analysis revealed that the overall bioelectrochemical performances of these reactors set them apart from all the other Panarea and Prony conditions, not only due to their higher current production but also archaeal abundances (measured through qPCR). Most reactors produced organic acids (up to 2.9 mM in 6 days). Still, coulombic efficiencies indicated that this might have been due to the (electro) fermentation of traces of yeast extract in the medium rather than CO2 fixation. Finally, microbial communities were described by 16S metabarcoding and ordination methods, and potential electrotrophic taxa were identified. In Panarea reactors, higher growth was correlated with a few bacterial genera, mainly Bacillus and Pseudoalteromonas, including, for the former, at higher temperatures (55°C and 75°C). In reactors reproducing the Prony Bay hydrothermal conditions, known facultative methylotrophs, such as Sphingomonas and Methylobacterium, were dominant and appeared to consume formate (provided as carbon source) but no electrons from the cathode.ConclusionThese results provide new insights into the distribution and diversity of electrotrophs in shallow-sea hydrothermal vents and allow the identification of potential novel biocatalysts for Microbial Electrosynthesis whereby electricity and carbon dioxide are converted into value-added products.https://www.frontiersin.org/articles/10.3389/fmicb.2025.1539608/fullhydrothermal ventselectrotrophsextremophilesthermophilesalkaliphilesbioelectrochemical reactors |
| spellingShingle | Antoine Carissimo Victoria Comes Alenica Heussner Anne-Hélène Prime Roy E. Price Gaël Erauso Pierre-Pol Liebgott Sven Kerzenmacher Guillaume Pillot Enrichment of electrotrophic microorganisms from contrasting shallow-sea hydrothermal environments in bioelectrochemical reactors Frontiers in Microbiology hydrothermal vents electrotrophs extremophiles thermophiles alkaliphiles bioelectrochemical reactors |
| title | Enrichment of electrotrophic microorganisms from contrasting shallow-sea hydrothermal environments in bioelectrochemical reactors |
| title_full | Enrichment of electrotrophic microorganisms from contrasting shallow-sea hydrothermal environments in bioelectrochemical reactors |
| title_fullStr | Enrichment of electrotrophic microorganisms from contrasting shallow-sea hydrothermal environments in bioelectrochemical reactors |
| title_full_unstemmed | Enrichment of electrotrophic microorganisms from contrasting shallow-sea hydrothermal environments in bioelectrochemical reactors |
| title_short | Enrichment of electrotrophic microorganisms from contrasting shallow-sea hydrothermal environments in bioelectrochemical reactors |
| title_sort | enrichment of electrotrophic microorganisms from contrasting shallow sea hydrothermal environments in bioelectrochemical reactors |
| topic | hydrothermal vents electrotrophs extremophiles thermophiles alkaliphiles bioelectrochemical reactors |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2025.1539608/full |
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