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

Yangkai Zhou1; An Yan2; Jiawen Yang2,3; Wei He1; Shuai Guo2,3; Yifan Li1; Jing Wu2; Yanchao Dai4; Xijiang Pan4; Dongyu Cui1; Olivier Pereira1,5; Wenkai Teng1; Ran Bi1; Songze Chen1; Lu Fan1; Peiyi Wang2; Yan Liao6; Wei Qin7; Sen-Fang Sui2,8; Yuanqing Zhu1,9; Chuanlun Zhang1,9,10; Zheng Liu2

2024-04-26

doi.org/10.3389/fmicb.2024.1367658

Frontiers in Microbiology   影响因子和分区

1664-302X

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.

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

SCI

英语

第一 ; 共同第一 ; 通讯

Stable Support Plan Program of Shenzhen Natural Science Fund[20200925173954005] ; National Natural Science Foundation of China["32241028","32393974","92351301"] ; Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Southern University of Science and Technology[ZDSYS201802081843490] ; Project of Educational Commission of Guangdong Province of China[2020KTSCX123]

Microbiology

Microbiology

WOS:001219647100001

FRONTIERS MEDIA SA

人工提交

正式出版

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

Yangkai Zhou,An Yan,Jiawen Yang,et al. Ultrastructural insights into cellular organization, energy storage and ribosomal dynamics of an ammonia-oxidizing archaeon from oligotrophic oceans[J]. Frontiers in Microbiology,2024,15:1367658.

Yangkai Zhou.,An Yan.,Jiawen Yang.,Wei He.,Shuai Guo.,...&Zheng Liu.(2024).Ultrastructural insights into cellular organization, energy storage and ribosomal dynamics of an ammonia-oxidizing archaeon from oligotrophic oceans.Frontiers in Microbiology,15,1367658.

Yangkai Zhou,et al."Ultrastructural insights into cellular organization, energy storage and ribosomal dynamics of an ammonia-oxidizing archaeon from oligotrophic oceans".Frontiers in Microbiology 15(2024):1367658.