Cell Structure Changes in the Hyperthermophilic Crenarchaeon <named-content content-type="genus-species">Sulfolobus islandicus</named-content> Lacking the S-Layer

ABSTRACT Rediscovery of the ancient evolutionary relationship between archaea and eukaryotes has revitalized interest in archaeal cell biology. Key to the understanding of archaeal cells is the surface layer (S-layer), which is commonly found in Archaea but whose in vivo function is unknown. Here, w...

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Autores principales:	Changyi Zhang, Rebecca L. Wipfler, Yuan Li, Zhiyu Wang, Emily N. Hallett, Rachel J. Whitaker
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Archaea cell structure Sulfolobus islandicus surface layer Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b143659a18a64590949116152426d04f
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spelling	oai:doaj.org-article:b143659a18a64590949116152426d04f2021-11-15T16:22:08ZCell Structure Changes in the Hyperthermophilic Crenarchaeon <named-content content-type="genus-species">Sulfolobus islandicus</named-content> Lacking the S-Layer10.1128/mBio.01589-192150-7511https://doaj.org/article/b143659a18a64590949116152426d04f2019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01589-19https://doaj.org/toc/2150-7511ABSTRACT Rediscovery of the ancient evolutionary relationship between archaea and eukaryotes has revitalized interest in archaeal cell biology. Key to the understanding of archaeal cells is the surface layer (S-layer), which is commonly found in Archaea but whose in vivo function is unknown. Here, we investigate the architecture and cellular roles of the S-layer in the hyperthermophilic crenarchaeon Sulfolobus islandicus. Electron micrographs of mutant cells lacking slaA or both slaA and slaB confirm the absence of the outermost layer (SlaA), whereas cells with intact or partially or completely detached SlaA are observed for the ΔslaB mutant. We experimentally identify a novel S-layer-associated protein, M164_1049, which does not functionally replace its homolog SlaB but likely assists SlaB to stabilize SlaA. Mutants deficient in the SlaA outer layer form large cell aggregates, and individual cell size varies, increasing significantly up to six times the diameter of wild-type cells. We show that the ΔslaA mutant cells exhibit more sensitivity to hyperosmotic stress but are not reduced to wild-type cell size. The ΔslaA mutant contains aberrant chromosome copy numbers not seen in wild-type cells, in which the cell cycle is tightly regulated. Together, these data suggest that the lack of SlaA results in either cell fusion or irregularities in cell division. Our studies show the key physiological and cellular functions of the S-layer in this archaeal cell. IMPORTANCE The S-layer is considered to be the sole component of the cell wall in Sulfolobales, a taxonomic group within the Crenarchaeota whose cellular features have been suggested to have a close relationship to the last archaea-eukaryote common ancestor. In this study, we genetically dissect how the two previously characterized S-layer genes as well as a newly identified S-layer-associated protein-encoding gene contribute to the S-layer architecture in Sulfolobus. We provide genetic evidence for the first time showing that the slaA gene is a key cell morphology determinant and may play a role in Sulfolobus cell division or/and cell fusion.Changyi ZhangRebecca L. WipflerYuan LiZhiyu WangEmily N. HallettRachel J. WhitakerAmerican Society for MicrobiologyarticleArchaeacell structureSulfolobus islandicussurface layerMicrobiologyQR1-502ENmBio, Vol 10, Iss 4 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Archaea cell structure Sulfolobus islandicus surface layer Microbiology QR1-502
spellingShingle	Archaea cell structure Sulfolobus islandicus surface layer Microbiology QR1-502 Changyi Zhang Rebecca L. Wipfler Yuan Li Zhiyu Wang Emily N. Hallett Rachel J. Whitaker Cell Structure Changes in the Hyperthermophilic Crenarchaeon <named-content content-type="genus-species">Sulfolobus islandicus</named-content> Lacking the S-Layer
description	ABSTRACT Rediscovery of the ancient evolutionary relationship between archaea and eukaryotes has revitalized interest in archaeal cell biology. Key to the understanding of archaeal cells is the surface layer (S-layer), which is commonly found in Archaea but whose in vivo function is unknown. Here, we investigate the architecture and cellular roles of the S-layer in the hyperthermophilic crenarchaeon Sulfolobus islandicus. Electron micrographs of mutant cells lacking slaA or both slaA and slaB confirm the absence of the outermost layer (SlaA), whereas cells with intact or partially or completely detached SlaA are observed for the ΔslaB mutant. We experimentally identify a novel S-layer-associated protein, M164_1049, which does not functionally replace its homolog SlaB but likely assists SlaB to stabilize SlaA. Mutants deficient in the SlaA outer layer form large cell aggregates, and individual cell size varies, increasing significantly up to six times the diameter of wild-type cells. We show that the ΔslaA mutant cells exhibit more sensitivity to hyperosmotic stress but are not reduced to wild-type cell size. The ΔslaA mutant contains aberrant chromosome copy numbers not seen in wild-type cells, in which the cell cycle is tightly regulated. Together, these data suggest that the lack of SlaA results in either cell fusion or irregularities in cell division. Our studies show the key physiological and cellular functions of the S-layer in this archaeal cell. IMPORTANCE The S-layer is considered to be the sole component of the cell wall in Sulfolobales, a taxonomic group within the Crenarchaeota whose cellular features have been suggested to have a close relationship to the last archaea-eukaryote common ancestor. In this study, we genetically dissect how the two previously characterized S-layer genes as well as a newly identified S-layer-associated protein-encoding gene contribute to the S-layer architecture in Sulfolobus. We provide genetic evidence for the first time showing that the slaA gene is a key cell morphology determinant and may play a role in Sulfolobus cell division or/and cell fusion.
format	article
author	Changyi Zhang Rebecca L. Wipfler Yuan Li Zhiyu Wang Emily N. Hallett Rachel J. Whitaker
author_facet	Changyi Zhang Rebecca L. Wipfler Yuan Li Zhiyu Wang Emily N. Hallett Rachel J. Whitaker
author_sort	Changyi Zhang
title	Cell Structure Changes in the Hyperthermophilic Crenarchaeon <named-content content-type="genus-species">Sulfolobus islandicus</named-content> Lacking the S-Layer
title_short	Cell Structure Changes in the Hyperthermophilic Crenarchaeon <named-content content-type="genus-species">Sulfolobus islandicus</named-content> Lacking the S-Layer
title_full	Cell Structure Changes in the Hyperthermophilic Crenarchaeon <named-content content-type="genus-species">Sulfolobus islandicus</named-content> Lacking the S-Layer
title_fullStr	Cell Structure Changes in the Hyperthermophilic Crenarchaeon <named-content content-type="genus-species">Sulfolobus islandicus</named-content> Lacking the S-Layer
title_full_unstemmed	Cell Structure Changes in the Hyperthermophilic Crenarchaeon <named-content content-type="genus-species">Sulfolobus islandicus</named-content> Lacking the S-Layer
title_sort	cell structure changes in the hyperthermophilic crenarchaeon <named-content content-type="genus-species">sulfolobus islandicus</named-content> lacking the s-layer
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/b143659a18a64590949116152426d04f
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Cell Structure Changes in the Hyperthermophilic Crenarchaeon <named-content content-type="genus-species">Sulfolobus islandicus</named-content> Lacking the S-Layer

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