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

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          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.

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          Most cited references79

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          MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability

          Kazutaka Katoh, Daron Standley (2013)
          We report a major update of the MAFFT multiple sequence alignment program. This version has several new features, including options for adding unaligned sequences into an existing alignment, adjustment of direction in nucleotide alignment, constrained alignment and parallel processing, which were implemented after the previous major update. This report shows actual examples to explain how these features work, alone and in combination. Some examples incorrectly aligned by MAFFT are also shown to clarify its limitations. We discuss how to avoid misalignments, and our ongoing efforts to overcome such limitations.
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            ModelFinder: Fast Model Selection for Accurate Phylogenetic Estimates

            Subha Kalyaanamoorthy, Bui Minh, Thomas Wong … (2017)
            Model-based molecular phylogenetics plays an important role in comparisons of genomic data, and model selection is a key step in all such analyses. We present ModelFinder, a fast model-selection method that greatly improves the accuracy of phylogenetic estimates. The improvement is achieved by incorporating a model of rate-heterogeneity across sites not previously considered in this context, and by allowing concurrent searches of model-space and tree-space.
            Article 0 comments Cited 4089 times – based on 0 reviews     Review now
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              IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era

              Bui Minh, Heiko Schmidt, Olga Chernomor … (2020)
              Abstract IQ-TREE (http://www.iqtree.org, last accessed February 6, 2020) is a user-friendly and widely used software package for phylogenetic inference using maximum likelihood. Since the release of version 1 in 2014, we have continuously expanded IQ-TREE to integrate a plethora of new models of sequence evolution and efficient computational approaches of phylogenetic inference to deal with genomic data. Here, we describe notable features of IQ-TREE version 2 and highlight the key advantages over other software.
              Article 0 comments Cited 3209 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Yangkai Zhou: URI : https://loop.frontiersin.org/people/1854990/overviewRole: Role: Role: Role: Role: Role: Role:
                An Yan: Role: Role: Role: Role: Role: Role: Role:
                Jiawen Yang: URI : https://loop.frontiersin.org/people/2625245/overviewRole: Role: Role: Role: Role: Role: Role: Role: Role:
                Wei He: URI : https://loop.frontiersin.org/people/1221792/overviewRole: Role: Role: Role: Role: Role: Role: Role:
                Shuai Guo: Role: Role: Role: Role: Role: Role: Role:
                Yifan Li: URI : https://loop.frontiersin.org/people/2710489/overviewRole: Role: Role:
                Jing Wu: Role: Role: Role: Role:
                Yanchao Dai: Role: Role: Role: Role: Role: Role:
                Xijiang Pan: Role: Role: Role: Role: Role: Role:
                Dongyu Cui: URI : https://loop.frontiersin.org/people/1975358/overviewRole: Role: Role:
                Olivier Pereira: URI : https://loop.frontiersin.org/people/2627615/overviewRole: Role: Role:
                Wenkai Teng: Role: Role: Role:
                Ran Bi: Role: Role: Role:
                Songze Chen: URI : https://loop.frontiersin.org/people/423464/overviewRole: Role: Role:
                Lu Fan: URI : https://loop.frontiersin.org/people/472798/overviewRole: Role: Role:
                Peiyi Wang: Role: Role: Role: Role:
                Yan Liao: URI : https://loop.frontiersin.org/people/1613610/overviewRole: Role: Role:
                Wei Qin: URI : https://loop.frontiersin.org/people/428268/overviewRole: Role: Role:
                Sen-Fang Sui: Role: Role: Role: Role: Role:
                Yuanqing Zhu: Role: Role: Role: Role:
                Chuanlun Zhang: URI : https://loop.frontiersin.org/people/22228/overviewRole: Role: Role: Role: Role: Role: Role: Role: Role:
                Zheng Liu: URI : https://loop.frontiersin.org/people/2620444/overviewRole: Role: Role: Role: Role: Role: Role: Role: Role:
                Journal
                Journal ID (nlm-ta): Front Microbiol
                Journal ID (iso-abbrev): Front Microbiol
                Journal ID (publisher-id): Front. Microbiol.
                Title: Frontiers in Microbiology
                Publisher: Frontiers Media S.A.
                ISSN (Electronic): 1664-302X
                Publication date (Electronic): 26 April 2024
                Publication date Collection: 2024
                Volume: 15
                Electronic Location Identifier: 1367658
                Affiliations
                [1] 1Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology , Shenzhen, Guangdong, China
                [2] 2Cryo-Electron Microscopy Center, Southern University of Science and Technology , Shenzhen, Guangdong, China
                [3] 3Department of Biology, Southern University of Science and Technology , Shenzhen, Guangdong, China
                [4] 4Shanghai NanoPort, Thermo Fisher Scientific Inc. , Shanghai, China
                [5] 5Institut AMU-WUT, Aix-Marseille Université and Wuhan University of Technology , Wuhan, Hubei, China
                [6] 6Australian Institute for Microbiology & Infection, University of Technology Sydney , Ultimo, NSW, Australia
                [7] 7School of Biological Sciences and Institute for Environmental Genomics, University of Oklahoma , Norman, OK, United States
                [8] 8State 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] 9Shanghai Sheshan National Geophysical Observatory , Shanghai, China
                [10] 10Advanced Institute for Ocean Research, Southern University of Science and Technology , Shenzhen, Guangdong, China
                Author notes

                Edited by: Ivan A. Berg, University of Münster, Germany

                Reviewed by: Reinhard Rachel, University of Regensburg, Germany

                Jeremy Dodsworth, California State University, San Bernardino, United States

                *Correspondence: Chuanlun Zhang, zhangcl@ 123456sustech.edu.cn

                †These authors have contributed equally to this work

                Article
                DOI: 10.3389/fmicb.2024.1367658
                PMC ID: 11082331
                SO-VID: c879e84e-2b1f-4691-bfbc-57ea618adf68
                Copyright © Copyright © 2024 Zhou, Yan, Yang, He, Guo, Li, Wu, Dai, Pan, Cui, Pereira, Teng, Bi, Chen, Fan, Wang, Liao, Qin, Sui, Zhu, Zhang and Liu.
                License:

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                Date received : 09 January 2024
                Date accepted : 16 April 2024
                Page count
                Figures: 5, Tables: 0, Equations: 0, References: 79, Pages: 12, Words: 8052
                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.
                Categories
                Subject: Microbiology
                Subject: Original Research
                Custom metadata
                section-at-acceptance Biology of Archaea

                ScienceOpen disciplines: Microbiology & Virology
                Keywords: ammonia-oxidizing archaeon,nitrosopumilus maritimus scm1,cryo-electron tomography (cryo-et),scanning transmission electron microscopy (stem),energy dispersive x-ray spectroscopy (eds)
                Data availability:
                ScienceOpen disciplines: Microbiology & Virology
                Keywords: ammonia-oxidizing archaeon, nitrosopumilus maritimus scm1, cryo-electron tomography (cryo-et), scanning transmission electron microscopy (stem), energy dispersive x-ray spectroscopy (eds)

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