Ultrastructural insights into cellular organization, energy storage and ribosomal dynamics of an ammonia-oxidizing archaeon from oligotrophic oceans

Yangkai Zhou; An Yan; Jiawen Yang; Jiawen Yang; Wei He; Shuai Guo; Shuai Guo; Yifan Li; Jing Wu; Yanchao Dai; Xijiang Pan; Dongyu Cui; Olivier Pereira; Olivier Pereira; Wenkai Teng; Ran Bi; Songze Chen; Lu Fan; Peiyi Wang; Yan Liao; Wei Qin; Sen-Fang Sui; Sen-Fang Sui; Yuanqing Zhu; Yuanqing Zhu; Chuanlun Zhang; Chuanlun Zhang; Chuanlun Zhang; Zheng Liu

doi:10.3389/fmicb.2024.1367658

Frontiers in Microbiology (Apr 2024)

Ultrastructural insights into cellular organization, energy storage and ribosomal dynamics of an ammonia-oxidizing archaeon from oligotrophic oceans

Yangkai Zhou,
An Yan,
Jiawen Yang,
Jiawen Yang,
Wei He,
Shuai Guo,
Shuai Guo,
Yifan Li,
Jing Wu,
Yanchao Dai,
Xijiang Pan,
Dongyu Cui,
Olivier Pereira,
Olivier Pereira,
Wenkai Teng,
Ran Bi,
Songze Chen,
Lu Fan,
Peiyi Wang,
Yan Liao,
Wei Qin,
Sen-Fang Sui,
Sen-Fang Sui,
Yuanqing Zhu,
Yuanqing Zhu,
Chuanlun Zhang,
Chuanlun Zhang,
Chuanlun Zhang,
Zheng Liu

Affiliations

Yangkai Zhou: Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, Guangdong, China
An Yan: Cryo-Electron Microscopy Center, Southern University of Science and Technology, Shenzhen, Guangdong, China
Jiawen Yang: Cryo-Electron Microscopy Center, Southern University of Science and Technology, Shenzhen, Guangdong, China
Jiawen Yang: Department of Biology, Southern University of Science and Technology, Shenzhen, Guangdong, China
Wei He: Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, Guangdong, China
Shuai Guo: Cryo-Electron Microscopy Center, Southern University of Science and Technology, Shenzhen, Guangdong, China
Shuai Guo: Department of Biology, Southern University of Science and Technology, Shenzhen, Guangdong, China
Yifan Li: Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, Guangdong, China
Jing Wu: Cryo-Electron Microscopy Center, Southern University of Science and Technology, Shenzhen, Guangdong, China
Yanchao Dai: Shanghai NanoPort, Thermo Fisher Scientific Inc., Shanghai, China
Xijiang Pan: Shanghai NanoPort, Thermo Fisher Scientific Inc., Shanghai, China
Dongyu Cui: Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, Guangdong, China
Olivier Pereira: Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, Guangdong, China
Olivier Pereira: Institut AMU-WUT, Aix-Marseille Université and Wuhan University of Technology, Wuhan, Hubei, China
Wenkai Teng: Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, Guangdong, China
Ran Bi: Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, Guangdong, China
Songze Chen: Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, Guangdong, China
Lu Fan: Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, Guangdong, China
Peiyi Wang: Cryo-Electron Microscopy Center, Southern University of Science and Technology, Shenzhen, Guangdong, China
Yan Liao: Australian Institute for Microbiology & Infection, University of Technology Sydney, Ultimo, NSW, Australia
Wei Qin: School of Biological Sciences and Institute for Environmental Genomics, University of Oklahoma, Norman, OK, United States
Sen-Fang Sui: Cryo-Electron Microscopy Center, Southern University of Science and Technology, Shenzhen, Guangdong, China
Sen-Fang Sui: State Key Laboratory of Membrane Biology, Beijing Frontier Research Center for Biological Structures, Beijing Advanced Innovation Center for Structural Biology, School of Life Sciences, Tsinghua University, Beijing, China
Yuanqing Zhu: Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, Guangdong, China
Yuanqing Zhu: Shanghai Sheshan National Geophysical Observatory, Shanghai, China
Chuanlun Zhang: Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, Guangdong, China
Chuanlun Zhang: Shanghai Sheshan National Geophysical Observatory, Shanghai, China
Chuanlun Zhang: 0Advanced Institute for Ocean Research, Southern University of Science and Technology, Shenzhen, Guangdong, China
Zheng Liu: Cryo-Electron Microscopy Center, Southern University of Science and Technology, Shenzhen, Guangdong, China

DOI: https://doi.org/10.3389/fmicb.2024.1367658
Journal volume & issue: Vol. 15

Abstract

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IntroductionNitrososphaeria, formerly known as Thaumarchaeota, constitute a diverse and widespread group of ammonia-oxidizing archaea (AOA) inhabiting ubiquitously in marine and terrestrial environments, playing a pivotal role in global nitrogen cycling. Despite their importance in Earth’s ecosystems, the cellular organization of AOA remains largely unexplored, leading to a significant unanswered question of how the machinery of these organisms underpins metabolic functions.MethodsIn this study, we combined spherical-chromatic-aberration-corrected cryo-electron tomography (cryo-ET), scanning transmission electron microscopy (STEM), and energy dispersive X-ray spectroscopy (EDS) to unveil the cellular organization and elemental composition of Nitrosopumilus maritimus SCM1, a representative member of marine Nitrososphaeria.Results and DiscussionOur tomograms show the native ultrastructural morphology of SCM1 and one to several dense storage granules in the cytoplasm. STEM-EDS analysis identifies two types of storage granules: one type is possibly composed of polyphosphate and the other polyhydroxyalkanoate. With precise measurements using cryo-ET, we observed low quantity and density of ribosomes in SCM1 cells, which are in alignment with the documented slow growth of AOA in laboratory cultures. Collectively, these findings provide visual evidence supporting the resilience of AOA in the vast oligotrophic marine environment.

Published in Frontiers in Microbiology

ISSN: 1664-302X (Online)
Publisher: Frontiers Media S.A.
Country of publisher: Switzerland
LCC subjects: Science: Microbiology
Website: http://www.frontiersin.org/journals/microbiology

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