The Polygonal Cell Shape and Surface Protein Layer of Anaerobic Methane-Oxidizing Methylomirabilislanthanidiphila Bacteria

Methylomirabilis bacteria perform anaerobic methane oxidation coupled to nitrite reduction via an intra-aerobic pathway, producing carbon dioxide and dinitrogen gas. These diderm bacteria possess an unusual polygonal cell shape with sharp ridges that run along the cell body. Previously, a putative s...

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Autores principales: Lavinia Gambelli, Rob Mesman, Wouter Versantvoort, Christoph A. Diebolder, Andreas Engel, Wiel Evers, Mike S. M. Jetten, Martin Pabst, Bertram Daum, Laura van Niftrik
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Publicado: Frontiers Media S.A. 2021
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spelling oai:doaj.org-article:41e14abb9c5d4abfbcaf7de17873aac52021-12-01T23:11:12ZThe Polygonal Cell Shape and Surface Protein Layer of Anaerobic Methane-Oxidizing Methylomirabilislanthanidiphila Bacteria1664-302X10.3389/fmicb.2021.766527https://doaj.org/article/41e14abb9c5d4abfbcaf7de17873aac52021-12-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fmicb.2021.766527/fullhttps://doaj.org/toc/1664-302XMethylomirabilis bacteria perform anaerobic methane oxidation coupled to nitrite reduction via an intra-aerobic pathway, producing carbon dioxide and dinitrogen gas. These diderm bacteria possess an unusual polygonal cell shape with sharp ridges that run along the cell body. Previously, a putative surface protein layer (S-layer) was observed as the outermost cell layer of these bacteria. We hypothesized that this S-layer is the determining factor for their polygonal cell shape. Therefore, we enriched the S-layer from M. lanthanidiphila cells and through LC-MS/MS identified a 31 kDa candidate S-layer protein, mela_00855, which had no homology to any other known protein. Antibodies were generated against a synthesized peptide derived from the mela_00855 protein sequence and used in immunogold localization to verify its identity and location. Both on thin sections of M. lanthanidiphila cells and in negative-stained enriched S-layer patches, the immunogold localization identified mela_00855 as the S-layer protein. Using electron cryo-tomography and sub-tomogram averaging of S-layer patches, we observed that the S-layer has a hexagonal symmetry. Cryo-tomography of whole cells showed that the S-layer and the outer membrane, but not the peptidoglycan layer and the cytoplasmic membrane, exhibited the polygonal shape. Moreover, the S-layer consisted of multiple rigid sheets that partially overlapped, most likely giving rise to the unique polygonal cell shape. These characteristics make the S-layer of M. lanthanidiphila a distinctive and intriguing case to study.Lavinia GambelliLavinia GambelliLavinia GambelliRob MesmanWouter VersantvoortChristoph A. DiebolderAndreas EngelWiel EversWiel EversMike S. M. JettenMartin PabstBertram DaumBertram DaumLaura van NiftrikFrontiers Media S.A.articleMethylomirabilisNC10 phylumanaerobic methane oxidationS-layercell shapecryo-tomographyMicrobiologyQR1-502ENFrontiers in Microbiology, Vol 12 (2021)
institution DOAJ
collection DOAJ
language EN
topic Methylomirabilis
NC10 phylum
anaerobic methane oxidation
S-layer
cell shape
cryo-tomography
Microbiology
QR1-502
spellingShingle Methylomirabilis
NC10 phylum
anaerobic methane oxidation
S-layer
cell shape
cryo-tomography
Microbiology
QR1-502
Lavinia Gambelli
Lavinia Gambelli
Lavinia Gambelli
Rob Mesman
Wouter Versantvoort
Christoph A. Diebolder
Andreas Engel
Wiel Evers
Wiel Evers
Mike S. M. Jetten
Martin Pabst
Bertram Daum
Bertram Daum
Laura van Niftrik
The Polygonal Cell Shape and Surface Protein Layer of Anaerobic Methane-Oxidizing Methylomirabilislanthanidiphila Bacteria
description Methylomirabilis bacteria perform anaerobic methane oxidation coupled to nitrite reduction via an intra-aerobic pathway, producing carbon dioxide and dinitrogen gas. These diderm bacteria possess an unusual polygonal cell shape with sharp ridges that run along the cell body. Previously, a putative surface protein layer (S-layer) was observed as the outermost cell layer of these bacteria. We hypothesized that this S-layer is the determining factor for their polygonal cell shape. Therefore, we enriched the S-layer from M. lanthanidiphila cells and through LC-MS/MS identified a 31 kDa candidate S-layer protein, mela_00855, which had no homology to any other known protein. Antibodies were generated against a synthesized peptide derived from the mela_00855 protein sequence and used in immunogold localization to verify its identity and location. Both on thin sections of M. lanthanidiphila cells and in negative-stained enriched S-layer patches, the immunogold localization identified mela_00855 as the S-layer protein. Using electron cryo-tomography and sub-tomogram averaging of S-layer patches, we observed that the S-layer has a hexagonal symmetry. Cryo-tomography of whole cells showed that the S-layer and the outer membrane, but not the peptidoglycan layer and the cytoplasmic membrane, exhibited the polygonal shape. Moreover, the S-layer consisted of multiple rigid sheets that partially overlapped, most likely giving rise to the unique polygonal cell shape. These characteristics make the S-layer of M. lanthanidiphila a distinctive and intriguing case to study.
format article
author Lavinia Gambelli
Lavinia Gambelli
Lavinia Gambelli
Rob Mesman
Wouter Versantvoort
Christoph A. Diebolder
Andreas Engel
Wiel Evers
Wiel Evers
Mike S. M. Jetten
Martin Pabst
Bertram Daum
Bertram Daum
Laura van Niftrik
author_facet Lavinia Gambelli
Lavinia Gambelli
Lavinia Gambelli
Rob Mesman
Wouter Versantvoort
Christoph A. Diebolder
Andreas Engel
Wiel Evers
Wiel Evers
Mike S. M. Jetten
Martin Pabst
Bertram Daum
Bertram Daum
Laura van Niftrik
author_sort Lavinia Gambelli
title The Polygonal Cell Shape and Surface Protein Layer of Anaerobic Methane-Oxidizing Methylomirabilislanthanidiphila Bacteria
title_short The Polygonal Cell Shape and Surface Protein Layer of Anaerobic Methane-Oxidizing Methylomirabilislanthanidiphila Bacteria
title_full The Polygonal Cell Shape and Surface Protein Layer of Anaerobic Methane-Oxidizing Methylomirabilislanthanidiphila Bacteria
title_fullStr The Polygonal Cell Shape and Surface Protein Layer of Anaerobic Methane-Oxidizing Methylomirabilislanthanidiphila Bacteria
title_full_unstemmed The Polygonal Cell Shape and Surface Protein Layer of Anaerobic Methane-Oxidizing Methylomirabilislanthanidiphila Bacteria
title_sort polygonal cell shape and surface protein layer of anaerobic methane-oxidizing methylomirabilislanthanidiphila bacteria
publisher Frontiers Media S.A.
publishDate 2021
url https://doaj.org/article/41e14abb9c5d4abfbcaf7de17873aac5
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