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

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

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

Afiliación

Zhou Y; Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, Guangdong, China.
Yan A; Cryo-Electron Microscopy Center, Southern University of Science and Technology, Shenzhen, Guangdong, China.
Yang J; Cryo-Electron Microscopy Center, Southern University of Science and Technology, Shenzhen, Guangdong, China.
He W; Department of Biology, Southern University of Science and Technology, Shenzhen, Guangdong, China.
Guo S; Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, Guangdong, China.
Li Y; Cryo-Electron Microscopy Center, Southern University of Science and Technology, Shenzhen, Guangdong, China.
Wu J; Department of Biology, Southern University of Science and Technology, Shenzhen, Guangdong, China.
Dai Y; Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, Guangdong, China.
Pan X; Cryo-Electron Microscopy Center, Southern University of Science and Technology, Shenzhen, Guangdong, China.
Cui D; Shanghai NanoPort, Thermo Fisher Scientific Inc., Shanghai, China.
Pereira O; Shanghai NanoPort, Thermo Fisher Scientific Inc., Shanghai, China.
Teng W; Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, Guangdong, China.
Bi R; Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, Guangdong, China.
Chen S; Institut AMU-WUT, Aix-Marseille Université and Wuhan University of Technology, Wuhan, Hubei, China.
Fan L; Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, Guangdong, China.
Wang P; Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, Guangdong, China.
Liao Y; Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, Guangdong, China.
Qin W; Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, Guangdong, China.
Sui SF; Cryo-Electron Microscopy Center, Southern University of Science and Technology, Shenzhen, Guangdong, China.
Zhu Y; Australian Institute for Microbiology & Infection, University of Technology Sydney, Ultimo, NSW, Australia.
Zhang C; School of Biological Sciences and Institute for Environmental Genomics, University of Oklahoma, Norman, OK, United States.
Liu Z; Cryo-Electron Microscopy Center, Southern University of Science and Technology, Shenzhen, Guangdong, China.

Front Microbiol ; 15: 1367658, 2024.

Article en En | MEDLINE | ID: mdl-38737410

ABSTRACT

ABSTRACT

Introduction:

Nitrososphaeria, 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.

Methods:

In 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

Discussion:

Our 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.

Palabras clave

Nitrosopumilus maritimus SCM1; ammonia-oxidizing archaeon; cryo-electron tomography (cryo-ET); energy dispersive X-ray spectroscopy (EDS); scanning transmission electron microscopy (STEM)

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