Cryptosporulation in Kurthia spp. forces a rethinking of asporogenesis in Firmicutes.


Journal

Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692

Informations de publication

Date de publication:
12 2022
Historique:
received: 19 06 2020
accepted: 20 07 2022
entrez: 19 12 2022
pubmed: 20 12 2022
medline: 21 12 2022
Statut: ppublish

Résumé

Endosporulation is a complex morphophysiological process resulting in a more resistant cellular structure that is produced within the mother cell and is called endospore. Endosporulation evolved in the common ancestor of Firmicutes, but it is lost in descendant lineages classified as asporogenic. While Kurthia spp. is considered to comprise only asporogenic species, we show here that strain 11kri321, which was isolated from an oligotrophic geothermal reservoir, produces phase-bright spore-like structures. Phylogenomics of strain 11kri321 and other Kurthia strains reveals little similarity to genetic determinants of sporulation known from endosporulating Bacilli. However, morphological hallmarks of endosporulation were observed in two of the four Kurthia strains tested, resulting in spore-like structures (cryptospores). In contrast to classic endospores, these cryptospores did not protect against heat or UV damage and successive sub-culturing led to the loss of the cryptosporulating phenotype. Our findings imply that a cryptosporulation phenotype may have been prevalent and subsequently lost by laboratory culturing in other Firmicutes currently considered as asporogenic. Cryptosporulation might thus represent an ancestral but unstable and adaptive developmental state in Firmicutes that is under selection under harsh environmental conditions.

Identifiants

pubmed: 36530021
doi: 10.1111/1462-2920.16145
pmc: PMC10086788
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

6320-6335

Informations de copyright

© 2022 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.

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Auteurs

Mathilda Fatton (M)

Laboratory of Microbiology, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland.

Sevasti Filippidou (S)

Laboratory of Microbiology, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland.
AstrobiologyOU, The Open University, Milton Keynes, UK.

Thomas Junier (T)

Laboratory of Microbiology, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland.
Vital-IT group, Swiss Institute of Bioinformatics, Lausanne, Switzerland.

Guillaume Cailleau (G)

Laboratory of Microbiology, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland.

Matthieu Berge (M)

Department of Microbiology and Molecular Medicine, Faculty of Medicine, University of Geneva, Geneva, Switzerland.

Daniel Poppleton (D)

Unité de Biologie Moléculaire du Gène chez les Extrémophiles, Département de Microbiologie, Institut Pasteur, France.

Thorsten B Blum (TB)

Biology and Chemistry, Laboratory of Biomolecular Research, Paul Scherrer Institute (PSI), Villigen, Switzerland.

Marek Kaminek (M)

Institute for Anatomy, University of Bern, Bern, Switzerland.

Adolfo Odriozola (A)

Institute for Anatomy, University of Bern, Bern, Switzerland.

Jochen Blom (J)

Bioinformatics and Systems Biology, Justus-Liebig-University Giessen, Giessen, Germany.

Shannon L Johnson (SL)

Bioscience Division, Los Alamos National Laboratory, Los Alamos, New Mexico, USA.

Jan Pieter Abrahams (JP)

Biology and Chemistry, Laboratory of Biomolecular Research, Paul Scherrer Institute (PSI), Villigen, Switzerland.
Center for Cellular Imaging and NanoAnalytics (C-CINA), Biozentrum, University of Basel, Basel, Switzerland.
Institute of Biology, Leiden University, Leiden, The Netherlands.

Patrick S Chain (PS)

Institute for Anatomy, University of Bern, Bern, Switzerland.

Simonetta Gribaldo (S)

Unité de Biologie Moléculaire du Gène chez les Extrémophiles, Département de Microbiologie, Institut Pasteur, France.

Elitza I Tocheva (EI)

Department of Microbiology and Immunology, Life Sciences Institute, University of British Columbia, Vancouver, British Columbia, Canada.

Benoît Zuber (B)

Institute for Anatomy, University of Bern, Bern, Switzerland.

Patrick H Viollier (PH)

Department of Microbiology and Molecular Medicine, Faculty of Medicine, University of Geneva, Geneva, Switzerland.

Pilar Junier (P)

Laboratory of Microbiology, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland.

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Classifications MeSH