Disproportionation of Inorganic Sulfur Compounds by Mesophilic Chemolithoautotrophic Campylobacterota
ABSTRACT The disproportionation of inorganic sulfur compounds could be widespread in natural habitats, and microorganisms could produce energy to support primary productivity through this catabolism. However, the microorganisms that carry this process out and the catabolic pathways at work remain re...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-02-01
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| Series: | mSystems |
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| Online Access: | https://journals.asm.org/doi/10.1128/msystems.00954-22 |
| _version_ | 1797895813407440896 |
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| author | Shasha Wang Lijing Jiang Shaobin Xie Karine Alain Zhaodi Wang Jun Wang Delin Liu Zongze Shao |
| author_facet | Shasha Wang Lijing Jiang Shaobin Xie Karine Alain Zhaodi Wang Jun Wang Delin Liu Zongze Shao |
| author_sort | Shasha Wang |
| collection | DOAJ |
| description | ABSTRACT The disproportionation of inorganic sulfur compounds could be widespread in natural habitats, and microorganisms could produce energy to support primary productivity through this catabolism. However, the microorganisms that carry this process out and the catabolic pathways at work remain relatively unstudied. Here, we investigated the bacterial diversity involved in sulfur disproportionation in hydrothermal plumes from Carlsberg Ridge in the northwestern Indian Ocean by enrichment cultures. A bacterial community analysis revealed that bacteria of the genera Sulfurimonas and Sulfurovum, belonging to the phylum Campylobacterota and previously having been characterized as chemolithoautotrophic sulfur oxidizers, were the most dominant members in six enrichment cultures. Subsequent bacterial isolation and physiological studies confirmed that five Sulfurimonas and Sulfurovum isolates could disproportionate thiosulfate and elemental sulfur. The ability to disproportionate sulfur was also demonstrated in several strains of Sulfurimonas and Sulfurovum that were isolated from hydrothermal vents or other natural environments. Dialysis membrane experiments showed that S0 disproportionation did not require the direct contact of cells with bulk sulfur. A comparative genomic analysis showed that Campylobacterota strains did not contain some genes of the Dsr and rDSR pathways (aprAB, dsrAB, dsrC, dsrMKJOP, and qmoABC) that are involved in sulfur disproportionation in some other taxa, suggesting the existence of an unrevealed catabolic pathway for sulfur disproportionation. These findings provide evidence for the catabolic versatility of these Campylobacterota genera, which are widely distributed in chemosynthetic environments, and expand our knowledge of the microbial taxa involved in this reaction of the biogeochemical sulfur cycle in hydrothermal vent environments. IMPORTANCE The phylum Campylobacterota, notably represented by the genera Sulfurimonas and Sulfurovum, is ubiquitous and predominant in deep-sea hydrothermal systems. It is well-known to be the major chemolithoautotrophic sulfur-oxidizing group in these habitats. Herein, we show that the mesophilic predominant chemolithoautotrophs of the genera Sulfurimonas and Sulfurovum could grow via sulfur disproportionation to gain energy. This is the first report of the chemolithoautotrophic disproportionation of thiosulfate and elemental sulfur within the genera Sulfurimonas and Sulfurovum, and this comes in addition to their already known role in the chemolithoautotrophic oxidation of sulfur compounds. Sulfur disproportionation via chemolithoautotrophic Campylobacterota may represent a previously unrecognized primary production process in hydrothermal vent ecosystems. |
| first_indexed | 2024-04-10T07:31:39Z |
| format | Article |
| id | doaj.art-02f2dcde373f41cbab7b2220828809b6 |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-04-10T07:31:39Z |
| publishDate | 2023-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-02f2dcde373f41cbab7b2220828809b62023-02-23T14:01:37ZengAmerican Society for MicrobiologymSystems2379-50772023-02-018110.1128/msystems.00954-22Disproportionation of Inorganic Sulfur Compounds by Mesophilic Chemolithoautotrophic CampylobacterotaShasha Wang0Lijing Jiang1Shaobin Xie2Karine Alain3Zhaodi Wang4Jun Wang5Delin Liu6Zongze Shao7Key Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources of China, Sino-French Laboratory of Deep-Sea Microbiology (MicrobSea), Xiamen, People’s Republic of ChinaKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources of China, Sino-French Laboratory of Deep-Sea Microbiology (MicrobSea), Xiamen, People’s Republic of ChinaKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources of China, Sino-French Laboratory of Deep-Sea Microbiology (MicrobSea), Xiamen, People’s Republic of ChinaCNRS, Univ Brest, Ifremer, Unité Biologie et Ecologie des Ecosystèmes Marins Profonds BEEP, UMR 6197, IRP 1211 MicrobSea, IUEM, Plouzané, FranceKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources of China, Sino-French Laboratory of Deep-Sea Microbiology (MicrobSea), Xiamen, People’s Republic of ChinaKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources of China, Sino-French Laboratory of Deep-Sea Microbiology (MicrobSea), Xiamen, People’s Republic of ChinaKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources of China, Sino-French Laboratory of Deep-Sea Microbiology (MicrobSea), Xiamen, People’s Republic of ChinaKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources of China, Sino-French Laboratory of Deep-Sea Microbiology (MicrobSea), Xiamen, People’s Republic of ChinaABSTRACT The disproportionation of inorganic sulfur compounds could be widespread in natural habitats, and microorganisms could produce energy to support primary productivity through this catabolism. However, the microorganisms that carry this process out and the catabolic pathways at work remain relatively unstudied. Here, we investigated the bacterial diversity involved in sulfur disproportionation in hydrothermal plumes from Carlsberg Ridge in the northwestern Indian Ocean by enrichment cultures. A bacterial community analysis revealed that bacteria of the genera Sulfurimonas and Sulfurovum, belonging to the phylum Campylobacterota and previously having been characterized as chemolithoautotrophic sulfur oxidizers, were the most dominant members in six enrichment cultures. Subsequent bacterial isolation and physiological studies confirmed that five Sulfurimonas and Sulfurovum isolates could disproportionate thiosulfate and elemental sulfur. The ability to disproportionate sulfur was also demonstrated in several strains of Sulfurimonas and Sulfurovum that were isolated from hydrothermal vents or other natural environments. Dialysis membrane experiments showed that S0 disproportionation did not require the direct contact of cells with bulk sulfur. A comparative genomic analysis showed that Campylobacterota strains did not contain some genes of the Dsr and rDSR pathways (aprAB, dsrAB, dsrC, dsrMKJOP, and qmoABC) that are involved in sulfur disproportionation in some other taxa, suggesting the existence of an unrevealed catabolic pathway for sulfur disproportionation. These findings provide evidence for the catabolic versatility of these Campylobacterota genera, which are widely distributed in chemosynthetic environments, and expand our knowledge of the microbial taxa involved in this reaction of the biogeochemical sulfur cycle in hydrothermal vent environments. IMPORTANCE The phylum Campylobacterota, notably represented by the genera Sulfurimonas and Sulfurovum, is ubiquitous and predominant in deep-sea hydrothermal systems. It is well-known to be the major chemolithoautotrophic sulfur-oxidizing group in these habitats. Herein, we show that the mesophilic predominant chemolithoautotrophs of the genera Sulfurimonas and Sulfurovum could grow via sulfur disproportionation to gain energy. This is the first report of the chemolithoautotrophic disproportionation of thiosulfate and elemental sulfur within the genera Sulfurimonas and Sulfurovum, and this comes in addition to their already known role in the chemolithoautotrophic oxidation of sulfur compounds. Sulfur disproportionation via chemolithoautotrophic Campylobacterota may represent a previously unrecognized primary production process in hydrothermal vent ecosystems.https://journals.asm.org/doi/10.1128/msystems.00954-22sulfur disproportionationCampylobacterotahydrothermal ventchemolithoautotroph |
| spellingShingle | Shasha Wang Lijing Jiang Shaobin Xie Karine Alain Zhaodi Wang Jun Wang Delin Liu Zongze Shao Disproportionation of Inorganic Sulfur Compounds by Mesophilic Chemolithoautotrophic Campylobacterota mSystems sulfur disproportionation Campylobacterota hydrothermal vent chemolithoautotroph |
| title | Disproportionation of Inorganic Sulfur Compounds by Mesophilic Chemolithoautotrophic Campylobacterota |
| title_full | Disproportionation of Inorganic Sulfur Compounds by Mesophilic Chemolithoautotrophic Campylobacterota |
| title_fullStr | Disproportionation of Inorganic Sulfur Compounds by Mesophilic Chemolithoautotrophic Campylobacterota |
| title_full_unstemmed | Disproportionation of Inorganic Sulfur Compounds by Mesophilic Chemolithoautotrophic Campylobacterota |
| title_short | Disproportionation of Inorganic Sulfur Compounds by Mesophilic Chemolithoautotrophic Campylobacterota |
| title_sort | disproportionation of inorganic sulfur compounds by mesophilic chemolithoautotrophic campylobacterota |
| topic | sulfur disproportionation Campylobacterota hydrothermal vent chemolithoautotroph |
| url | https://journals.asm.org/doi/10.1128/msystems.00954-22 |
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