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

• Published in: Environmental microbiology 2022-12, Vol.24 (12), p.6320-6335
• Main Authors: Fatton, Mathilda, Filippidou, Sevasti, Junier, Thomas, Cailleau, Guillaume, Berge, Matthieu, Poppleton, Daniel, Blum, Thorsten B., Kaminek, Marek, Odriozola, Adolfo, Blom, Jochen, Johnson, Shannon L., Abrahams, Jan Pieter, Chain, Patrick S., Gribaldo, Simonetta, Tocheva, Elitza I., Zuber, Benoît, Viollier, Patrick H., Junier, Pilar
• Format: Article
• Language: English
• Subjects: Bacilli; Bacillus; BASIC BIOLOGICAL SCIENCES; Cellular structure; Environmental conditions; Firmicutes; Microbiology; Phenotypes; Phylogeny; Spores; Spores, Bacterial - genetics; Sporulation
• ISSN: 1462-2912; 1462-2920
• DOI: 10.1111/1462-2920.16145

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.