Metagenomic Discovery of “Candidatus Parvarchaeales”-Related Lineages Sheds Light on Adaptation and Diversification from Neutral-Thermal to Acidic-Mesothermal Environments
ABSTRACT “Candidatus Parvarchaeales” microbes, representing a DPANN archaeal group with limited metabolic potential and reliance on hosts for their growth, were initially found in acid mine drainage (AMD). Due to the lack of representatives, however, their ecological roles and adaptation to extreme...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-04-01
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| Series: | mSystems |
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| Online Access: | https://journals.asm.org/doi/10.1128/msystems.01252-22 |
| _version_ | 1827150135831822336 |
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| author | Yang-Zhi Rao Yu-Xian Li Ze-Wei Li Yan-Ni Qu Yan-Ling Qi Jian-Yu Jiao Wen-Sheng Shu Zheng-Shuang Hua Wen-Jun Li |
| author_facet | Yang-Zhi Rao Yu-Xian Li Ze-Wei Li Yan-Ni Qu Yan-Ling Qi Jian-Yu Jiao Wen-Sheng Shu Zheng-Shuang Hua Wen-Jun Li |
| author_sort | Yang-Zhi Rao |
| collection | DOAJ |
| description | ABSTRACT “Candidatus Parvarchaeales” microbes, representing a DPANN archaeal group with limited metabolic potential and reliance on hosts for their growth, were initially found in acid mine drainage (AMD). Due to the lack of representatives, however, their ecological roles and adaptation to extreme habitats such as AMD as well as how they diverge across the lineage remain largely unexplored. By applying genome-resolved metagenomics, 28 Parvarchaeales-associated metagenome-assembled genomes (MAGs) representing two orders and five genera were recovered. Among them, we identified three new genera and proposed the names “Candidatus Jingweiarchaeum,” “Candidatus Haiyanarchaeum,” and “Candidatus Rehaiarchaeum,” with the former two belonging to a new order, “Candidatus Jingweiarchaeales.” Further analyses of the metabolic potentials revealed substantial niche differentiation between Jingweiarchaeales and Parvarchaeales. Jingweiarchaeales may rely on fermentation, salvage pathways, partial glycolysis, and the pentose phosphate pathway (PPP) for energy conservation reservation, while the metabolic potentials of Parvarchaeales might be more versatile. Comparative genomic analyses suggested that Jingweiarchaeales favor habitats with higher temperatures and that Parvarchaeales are better adapted to acidic environments. We further revealed that the thermal adaptation of these lineages, especially Haiyanarchaeum, might rely on genomic features such as the usage of specific amino acids, genome streamlining, and hyperthermophile featured genes such as rgy. Notably, the adaptation of Parvarchaeales to acidic environments was possibly driven by horizontal gene transfer (HGT). The reconstruction of ancestral states demonstrated that both may have originated from thermal and neutral environments and later spread to mesothermal and acidic environments. These evolutionary processes may also be accompanied by adaptation to oxygen-rich environments via HGT. IMPORTANCE “Candidatus Parvarchaeales” microbes may represent a lineage uniquely distributed in extreme environments such as AMD and hot springs. However, little is known about the strategies and processes of how they adapted to these extreme environments. By the discovery of potential new order-level lineages, “Ca. Jingweiarchaeales,” and in-depth comparative genomic analysis, we unveiled the functional differentiation of these lineages. Furthermore, we show that the adaptation of these lineages to high-temperature and acidic environments was driven by different strategies, with the former relying more on genomic characteristics such as genome streamlining and amino acid compositions and the latter relying more on the acquisition of genes associated with acid tolerance. Finally, by the reconstruction of the ancestral states of the optimal growth temperature (OGT) and isoelectric point (pI), we showed the potential evolutionary process of Parvarchaeales-related lineages with regard to the shift from the high-temperature environment of their common ancestors to low-temperature (potentially acidic) environments. |
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| language | English |
| last_indexed | 2025-03-20T21:29:16Z |
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| spelling | doaj.art-d310f9bf0a074b3281656383b4ed3b162024-08-11T18:54:34ZengAmerican Society for MicrobiologymSystems2379-50772023-04-018210.1128/msystems.01252-22Metagenomic Discovery of “Candidatus Parvarchaeales”-Related Lineages Sheds Light on Adaptation and Diversification from Neutral-Thermal to Acidic-Mesothermal EnvironmentsYang-Zhi Rao0Yu-Xian Li1Ze-Wei Li2Yan-Ni Qu3Yan-Ling Qi4Jian-Yu Jiao5Wen-Sheng Shu6Zheng-Shuang Hua7Wen-Jun Li8State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-Sen University, Guangzhou, People’s Republic of ChinaChinese Academy of Sciences Key Laboratory of Urban Pollutant Conversion, Department of Environmental Science and Engineering, University of Science and Technology of China, Hefei, People’s Republic of ChinaChinese Academy of Sciences Key Laboratory of Urban Pollutant Conversion, Department of Environmental Science and Engineering, University of Science and Technology of China, Hefei, People’s Republic of ChinaState Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-Sen University, Guangzhou, People’s Republic of ChinaChinese Academy of Sciences Key Laboratory of Urban Pollutant Conversion, Department of Environmental Science and Engineering, University of Science and Technology of China, Hefei, People’s Republic of ChinaState Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-Sen University, Guangzhou, People’s Republic of ChinaSchool of Life Sciences, South China Normal University, Guangzhou, People’s Republic of ChinaChinese Academy of Sciences Key Laboratory of Urban Pollutant Conversion, Department of Environmental Science and Engineering, University of Science and Technology of China, Hefei, People’s Republic of ChinaState Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-Sen University, Guangzhou, People’s Republic of ChinaABSTRACT “Candidatus Parvarchaeales” microbes, representing a DPANN archaeal group with limited metabolic potential and reliance on hosts for their growth, were initially found in acid mine drainage (AMD). Due to the lack of representatives, however, their ecological roles and adaptation to extreme habitats such as AMD as well as how they diverge across the lineage remain largely unexplored. By applying genome-resolved metagenomics, 28 Parvarchaeales-associated metagenome-assembled genomes (MAGs) representing two orders and five genera were recovered. Among them, we identified three new genera and proposed the names “Candidatus Jingweiarchaeum,” “Candidatus Haiyanarchaeum,” and “Candidatus Rehaiarchaeum,” with the former two belonging to a new order, “Candidatus Jingweiarchaeales.” Further analyses of the metabolic potentials revealed substantial niche differentiation between Jingweiarchaeales and Parvarchaeales. Jingweiarchaeales may rely on fermentation, salvage pathways, partial glycolysis, and the pentose phosphate pathway (PPP) for energy conservation reservation, while the metabolic potentials of Parvarchaeales might be more versatile. Comparative genomic analyses suggested that Jingweiarchaeales favor habitats with higher temperatures and that Parvarchaeales are better adapted to acidic environments. We further revealed that the thermal adaptation of these lineages, especially Haiyanarchaeum, might rely on genomic features such as the usage of specific amino acids, genome streamlining, and hyperthermophile featured genes such as rgy. Notably, the adaptation of Parvarchaeales to acidic environments was possibly driven by horizontal gene transfer (HGT). The reconstruction of ancestral states demonstrated that both may have originated from thermal and neutral environments and later spread to mesothermal and acidic environments. These evolutionary processes may also be accompanied by adaptation to oxygen-rich environments via HGT. IMPORTANCE “Candidatus Parvarchaeales” microbes may represent a lineage uniquely distributed in extreme environments such as AMD and hot springs. However, little is known about the strategies and processes of how they adapted to these extreme environments. By the discovery of potential new order-level lineages, “Ca. Jingweiarchaeales,” and in-depth comparative genomic analysis, we unveiled the functional differentiation of these lineages. Furthermore, we show that the adaptation of these lineages to high-temperature and acidic environments was driven by different strategies, with the former relying more on genomic characteristics such as genome streamlining and amino acid compositions and the latter relying more on the acquisition of genes associated with acid tolerance. Finally, by the reconstruction of the ancestral states of the optimal growth temperature (OGT) and isoelectric point (pI), we showed the potential evolutionary process of Parvarchaeales-related lineages with regard to the shift from the high-temperature environment of their common ancestors to low-temperature (potentially acidic) environments.https://journals.asm.org/doi/10.1128/msystems.01252-22archaeaDPANNthermophilyancestral traits |
| spellingShingle | Yang-Zhi Rao Yu-Xian Li Ze-Wei Li Yan-Ni Qu Yan-Ling Qi Jian-Yu Jiao Wen-Sheng Shu Zheng-Shuang Hua Wen-Jun Li Metagenomic Discovery of “Candidatus Parvarchaeales”-Related Lineages Sheds Light on Adaptation and Diversification from Neutral-Thermal to Acidic-Mesothermal Environments mSystems archaea DPANN thermophily ancestral traits |
| title | Metagenomic Discovery of “Candidatus Parvarchaeales”-Related Lineages Sheds Light on Adaptation and Diversification from Neutral-Thermal to Acidic-Mesothermal Environments |
| title_full | Metagenomic Discovery of “Candidatus Parvarchaeales”-Related Lineages Sheds Light on Adaptation and Diversification from Neutral-Thermal to Acidic-Mesothermal Environments |
| title_fullStr | Metagenomic Discovery of “Candidatus Parvarchaeales”-Related Lineages Sheds Light on Adaptation and Diversification from Neutral-Thermal to Acidic-Mesothermal Environments |
| title_full_unstemmed | Metagenomic Discovery of “Candidatus Parvarchaeales”-Related Lineages Sheds Light on Adaptation and Diversification from Neutral-Thermal to Acidic-Mesothermal Environments |
| title_short | Metagenomic Discovery of “Candidatus Parvarchaeales”-Related Lineages Sheds Light on Adaptation and Diversification from Neutral-Thermal to Acidic-Mesothermal Environments |
| title_sort | metagenomic discovery of candidatus parvarchaeales related lineages sheds light on adaptation and diversification from neutral thermal to acidic mesothermal environments |
| topic | archaea DPANN thermophily ancestral traits |
| url | https://journals.asm.org/doi/10.1128/msystems.01252-22 |
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