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Diversity and salinity adaptations of ammonia oxidizing archaea in three estuaries of China

  • Genomics, Transcriptomics, Proteomics
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Ammonia-oxidizing archaea (AOA) are ubiquitously found in diverse habitats and play pivotal roles in the nitrogen and carbon cycle, especially in estuarine and coastal environments. Despite the fact that the diversity and distribution of AOA are thought to be tightly linked to habitats, little is known about the relationship that underpins their genomic traits, adaptive potentials, and ecological niches. Here, we have characterized and compared the AOA community in three estuaries of China using metagenomics. AOA were the dominant ammonia oxidizers in the three estuaries. Through phylogenetic analyses, five major AOA groups were identified, including the Nitrosomarinus-like, Nitrosopumilus-like, Aestuariumsis-like, Nitrosarchaeum-like, and Nitrosopelagicus-like groups. Statistical analyses showed that the aquatic and sedimentary AOA communities were mainly influenced by spatial factors (latitude and water depth) and environmental factors (salinity, pH, and dissolved oxygen) in estuaries, respectively. Compared to AOA dwelling in terrestrial and marine habitats, estuarine AOA encoded more genes involved in glucose and amino acid metabolism, transport systems, osmotic control, and cell motility. The low proteome isoelectric points (pI), high content of acidic amino acids, and the presence of potassium ion and mechanosensitive channels suggest a “salt-in” strategy for estuarine AOA to counteract high osmolarity in their surroundings. Our findings have indicated potential adaptation strategies and highlighted their importance in the estuarine nitrogen and carbon cycles.

Key points

• Spatial and environmental factors influence water and sediment AOA respectively.

• Estuarine AOA share low proteome isoelectric value and high acid amino acids content.

• AOA adaptation to estuaries is likely resulted from their unique genomic features.

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Data availability

The raw reads for samples and reconstructed AOA MAGs from the CRE, the JRE, and the PRE are available in the National Omics Data Encyclopedia (NODE) database (http://www.biosino.org/node) under the Bioproject accession numbers OEP001524, OEP000961, and OEP004282, respectively.

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Funding

This work was supported by the National Natural Science Foundation of China (grant numbers 32225003, 31970105, 992251306, 42141003); the Shenzhen Science and Technology Program (grant number JCYJ20200109105010363); the Innovation Team Project of Universities in Guangdong Province (grant number 2020KCXTD023); Shenzhen University 2035 Program for Excellent Research (2022B002); the China Postdoctoral Science Foundation (grant number. 2022M722175); Long Term Observation and Research Plan in the Changjiang Estuary and the Adjacent East China Sea Project (LORCE) (grant number 14282); and the National Program on Global Change and Air-Sea Interaction (Phase II)—Hypoxia and Acidification Monitoring and Warning Project in the Changjiang Estuary. CZ also acknowledges supports from the Department of Science and Technology of Guangdong Province (grant number 2021B151512008), the Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Southern University of Science and Technology (grant number ZDSYS201802081843490), and the Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (grant number K19313901). HL acknowledges the support by the Hong Kong Branch of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (grant number SMSEGL20SC01).

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Authors and Affiliations

  1. Archaeal Biology Center, Institute for Advanced Study, Shenzhen University, Shenzhen, 518060, China

    Dayu Zou & Meng Li

  2. Shenzhen Key Laboratory of Marine Microbiome Engineering, Institute for Advanced Study, Shenzhen University, Shenzhen, 518060, China

    Dayu Zou & Meng Li

  3. Key Laboratory of Marine Ecosystem Dynamics, Second Institute of Oceanography, Ministry of Natural Resources, Hangzhou, 310012, China

    Jianfang Chen

  4. Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Southern University of Science and Technology, Shenzhen, 518000, China

    Chuanlun Zhang

  5. Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, 510000, China

    Chuanlun Zhang

  6. State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, 361000, China

    Shuh-Ji Kao

  7. Department of Ocean Science and Hong Kong Branch of Southern Marine Science & Engineering Guangdong Laboratory (Guangzhou), The Hong Kong University of Science and Technology, Hong Kong SAR, China

    Hongbin Liu

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  1. Dayu Zou
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  2. Jianfang Chen
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  4. Shuh-Ji Kao
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Contributions

DZ and ML conceptualized the study. JC, CZ, SK, and HL provided the samples. DZ performed laboratory work, collected the data, performed the analyses and wrote the manuscript with the help from all co-authors.

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Correspondence to Meng Li.

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Zou, D., Chen, J., Zhang, C. et al. Diversity and salinity adaptations of ammonia oxidizing archaea in three estuaries of China. Appl Microbiol Biotechnol 107, 6897–6909 (2023). https://doi.org/10.1007/s00253-023-12761-4

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  • DOI: https://doi.org/10.1007/s00253-023-12761-4

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