Genomic Evidence for the Recycling of Complex Organic Carbon by Novel Thermoplasmatota Clades in Deep-Sea Sediments
ABSTRACT Thermoplasmatota have been widely reported in a variety of ecosystems, but their distribution and ecological role in marine sediments are still elusive. Here, we obtained four draft genomes affiliated with the former RBG-16-68-12 clade, which is now considered a new order, “Candidatus Yapla...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2022-06-01
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| Series: | mSystems |
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| Online Access: | https://journals.asm.org/doi/10.1128/msystems.00077-22 |
| _version_ | 1818545547440553984 |
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| author | Peng-Fei Zheng Zhanfei Wei Yingli Zhou Qingmei Li Zhao Qi Xiaoping Diao Yong Wang |
| author_facet | Peng-Fei Zheng Zhanfei Wei Yingli Zhou Qingmei Li Zhao Qi Xiaoping Diao Yong Wang |
| author_sort | Peng-Fei Zheng |
| collection | DOAJ |
| description | ABSTRACT Thermoplasmatota have been widely reported in a variety of ecosystems, but their distribution and ecological role in marine sediments are still elusive. Here, we obtained four draft genomes affiliated with the former RBG-16-68-12 clade, which is now considered a new order, “Candidatus Yaplasmales,” of the Thermoplasmatota phylum in sediments from the South China Sea. The phylogenetic trees based on the 16S rRNA genes and draft genomes showed that “Ca. Yaplasmales” archaea are composed of three clades: A, B, and C. Among them, clades A and B are abundantly distributed (up to 10.86%) in the marine anoxic sediment layers (>10-cm depth) of six of eight cores from 1,200- to 3,400-m depths. Metabolic pathway reconstructions indicated that all clades of “Ca. Yaplasmales” have the capacity for alkane degradation by predicted alkyl-succinate synthase. Clade A of “Ca. Yaplasmales” might be mixotrophic microorganisms for the identification of the complete Wood-Ljungdahl pathway and putative genes involved in the degradation of aromatic and halogenated organic compounds. Clades B and C were likely heterotrophic, especially with the potential capacity of the spermidine/putrescine and aromatic compound degradation, as suggested by a significant negative correlation between the concentrations of aromatic compounds and the relative abundances of clade B. The sulfide-quinone oxidoreductase and pyrophosphate-energized membrane proton pump were encoded by all genomes of “Ca. Yaplasmales,” serving as adaptive strategies for energy production. These findings suggest that “Ca. Yaplasmales” might synergistically transform benthic pollutant and detrital organic matter, possibly playing a vital role in the marine and terrestrial sedimentary carbon cycle. IMPORTANCE Deep oceans receive large amounts of complex organic carbon and anthropogenic pollutants. The deep-sea sediments of the continental slopes serve as the biggest carbon sink on Earth. Particulate organic carbons and detrital proteins accumulate in the sediment. The microbially mediated recycling of complex organic carbon is still largely unknown, which is an important question for carbon budget in global oceans and maintenance of the deep-sea ecosystem. In this study, we report the prevalence (up to 10.86% of the microbial community) of archaea from a novel order of Thermoplasmatota, “Ca. Yaplasmales,” in six of eight cores from 1,200- to 3,400-m depths in the South China Sea. We provide genomic evidence of “Ca. Yaplasmales” in the anaerobic microbial degradation of alkanes, aliphatic and monoaromatic hydrocarbons, and halogenated organic compounds. Our study identifies the key archaeal players in anoxic marine sediments, which are probably critical in recycling the complex organic carbon in global oceans. |
| first_indexed | 2024-12-12T07:41:34Z |
| format | Article |
| id | doaj.art-b2ef382010a147d7ac38f638bc9c072d |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-12-12T07:41:34Z |
| publishDate | 2022-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-b2ef382010a147d7ac38f638bc9c072d2022-12-22T00:32:46ZengAmerican Society for MicrobiologymSystems2379-50772022-06-017310.1128/msystems.00077-22Genomic Evidence for the Recycling of Complex Organic Carbon by Novel Thermoplasmatota Clades in Deep-Sea SedimentsPeng-Fei Zheng0Zhanfei Wei1Yingli Zhou2Qingmei Li3Zhao Qi4Xiaoping Diao5Yong Wang6Institute of Deep Sea Science and Engineering, Chinese Academy of Sciences, Sanya, Hainan, ChinaInstitute of Deep Sea Science and Engineering, Chinese Academy of Sciences, Sanya, Hainan, ChinaInstitute of Deep Sea Science and Engineering, Chinese Academy of Sciences, Sanya, Hainan, ChinaInstitute of Deep Sea Science and Engineering, Chinese Academy of Sciences, Sanya, Hainan, ChinaState Key Laboratory of Marine Resources Utilization in the South China Sea, Hainan University, Haikou, ChinaState Key Laboratory of Marine Resources Utilization in the South China Sea, Hainan University, Haikou, ChinaInstitute of Deep Sea Science and Engineering, Chinese Academy of Sciences, Sanya, Hainan, ChinaABSTRACT Thermoplasmatota have been widely reported in a variety of ecosystems, but their distribution and ecological role in marine sediments are still elusive. Here, we obtained four draft genomes affiliated with the former RBG-16-68-12 clade, which is now considered a new order, “Candidatus Yaplasmales,” of the Thermoplasmatota phylum in sediments from the South China Sea. The phylogenetic trees based on the 16S rRNA genes and draft genomes showed that “Ca. Yaplasmales” archaea are composed of three clades: A, B, and C. Among them, clades A and B are abundantly distributed (up to 10.86%) in the marine anoxic sediment layers (>10-cm depth) of six of eight cores from 1,200- to 3,400-m depths. Metabolic pathway reconstructions indicated that all clades of “Ca. Yaplasmales” have the capacity for alkane degradation by predicted alkyl-succinate synthase. Clade A of “Ca. Yaplasmales” might be mixotrophic microorganisms for the identification of the complete Wood-Ljungdahl pathway and putative genes involved in the degradation of aromatic and halogenated organic compounds. Clades B and C were likely heterotrophic, especially with the potential capacity of the spermidine/putrescine and aromatic compound degradation, as suggested by a significant negative correlation between the concentrations of aromatic compounds and the relative abundances of clade B. The sulfide-quinone oxidoreductase and pyrophosphate-energized membrane proton pump were encoded by all genomes of “Ca. Yaplasmales,” serving as adaptive strategies for energy production. These findings suggest that “Ca. Yaplasmales” might synergistically transform benthic pollutant and detrital organic matter, possibly playing a vital role in the marine and terrestrial sedimentary carbon cycle. IMPORTANCE Deep oceans receive large amounts of complex organic carbon and anthropogenic pollutants. The deep-sea sediments of the continental slopes serve as the biggest carbon sink on Earth. Particulate organic carbons and detrital proteins accumulate in the sediment. The microbially mediated recycling of complex organic carbon is still largely unknown, which is an important question for carbon budget in global oceans and maintenance of the deep-sea ecosystem. In this study, we report the prevalence (up to 10.86% of the microbial community) of archaea from a novel order of Thermoplasmatota, “Ca. Yaplasmales,” in six of eight cores from 1,200- to 3,400-m depths in the South China Sea. We provide genomic evidence of “Ca. Yaplasmales” in the anaerobic microbial degradation of alkanes, aliphatic and monoaromatic hydrocarbons, and halogenated organic compounds. Our study identifies the key archaeal players in anoxic marine sediments, which are probably critical in recycling the complex organic carbon in global oceans.https://journals.asm.org/doi/10.1128/msystems.00077-22PAHarchaeaaromatic degradationanaerobesmetagenomedehalogenase |
| spellingShingle | Peng-Fei Zheng Zhanfei Wei Yingli Zhou Qingmei Li Zhao Qi Xiaoping Diao Yong Wang Genomic Evidence for the Recycling of Complex Organic Carbon by Novel Thermoplasmatota Clades in Deep-Sea Sediments mSystems PAH archaea aromatic degradation anaerobes metagenome dehalogenase |
| title | Genomic Evidence for the Recycling of Complex Organic Carbon by Novel Thermoplasmatota Clades in Deep-Sea Sediments |
| title_full | Genomic Evidence for the Recycling of Complex Organic Carbon by Novel Thermoplasmatota Clades in Deep-Sea Sediments |
| title_fullStr | Genomic Evidence for the Recycling of Complex Organic Carbon by Novel Thermoplasmatota Clades in Deep-Sea Sediments |
| title_full_unstemmed | Genomic Evidence for the Recycling of Complex Organic Carbon by Novel Thermoplasmatota Clades in Deep-Sea Sediments |
| title_short | Genomic Evidence for the Recycling of Complex Organic Carbon by Novel Thermoplasmatota Clades in Deep-Sea Sediments |
| title_sort | genomic evidence for the recycling of complex organic carbon by novel thermoplasmatota clades in deep sea sediments |
| topic | PAH archaea aromatic degradation anaerobes metagenome dehalogenase |
| url | https://journals.asm.org/doi/10.1128/msystems.00077-22 |
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