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

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

doi:10.3389/fmicb.2024.1367658

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

Front Microbiol. 2024 Apr 26:15:1367658. doi: 10.3389/fmicb.2024.1367658. eCollection 2024.

Authors

Yangkai Zhou^#¹, An Yan^#², Jiawen Yang^#^{2

3}, Wei He^#¹, Shuai Guo^{2

3}, Yifan Li¹, Jing Wu², Yanchao Dai⁴, Xijiang Pan⁴, Dongyu Cui¹, Olivier Pereira^{1

5}, Wenkai Teng¹, Ran Bi¹, Songze Chen¹, Lu Fan¹, Peiyi Wang², Yan Liao⁶, Wei Qin⁷, Sen-Fang Sui^{2

8}, Yuanqing Zhu^{1

9}, Chuanlun Zhang^{1

9

10}, Zheng Liu²

Affiliations

¹ Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, Guangdong, China.
² Cryo-Electron Microscopy Center, Southern University of Science and Technology, Shenzhen, Guangdong, China.
³ Department of Biology, Southern University of Science and Technology, Shenzhen, Guangdong, China.
⁴ Shanghai NanoPort, Thermo Fisher Scientific Inc., Shanghai, China.
⁵ Institut AMU-WUT, Aix-Marseille Université and Wuhan University of Technology, Wuhan, Hubei, China.
⁶ Australian Institute for Microbiology & Infection, University of Technology Sydney, Ultimo, NSW, Australia.
⁷ School of Biological Sciences and Institute for Environmental Genomics, University of Oklahoma, Norman, OK, United States.
⁸ 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.
⁹ Shanghai Sheshan National Geophysical Observatory, Shanghai, China.
¹⁰ Advanced Institute for Ocean Research, Southern University of Science and Technology, Shenzhen, Guangdong, China.

^# Contributed equally.

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.

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

Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This study was supported by the Stable Support Plan Program of Shenzhen Natural Science Fund (20200925173954005), National Natural Science Foundation of China (32241028, 32393974, and 92351301), the Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Southern University of Science and Technology (ZDSYS201802081843490), and the Project of Educational Commission of Guangdong Province of China (2020KTSCX123). The bioinformatic analyses were performed on the Tai-Yi high-performance supercomputer cluster at Southern University of Science and Technology.