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Pleomorphic Variants of Borreliella (syn. Borrelia) burgdorferi Express Evolutionary Distinct Transcriptomes

Čorak, Nina; Anniko, Sirli; Daschkin-Steinborn, Christina; Krey, Viktoria; Koska, Sara; Futo, Momir; Široki, Tin; Woichansky, Innokenty; Opašić, Luka; Kifer, Domagoj; Tušar, Anja; Maxeiner, Horst-Günter; Domazet-Lošo, Mirjana; Nicolaus, Carsten; Domazet-Lošo, Tomislav (2023) Pleomorphic Variants of Borreliella (syn. Borrelia) burgdorferi Express Evolutionary Distinct Transcriptomes. International journal of molecular sciences, 24 (6). ISSN 1422-0067

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Borreliella (syn. Borrelia) burgdorferi is a spirochete bacterium that causes tick-borne Lyme disease. Along its lifecycle B. burgdorferi develops several pleomorphic forms with unclear biological and medical relevance. Surprisingly, these morphotypes have never been compared at the global transcriptome level. To fill this void, we grew B. burgdorferi spirochete, round body, bleb, and biofilm- dominated cultures and recovered their transcriptomes by RNAseq profiling. We found that round bodies share similar expression profiles with spirochetes, despite their morphological differences. This sharply contrasts to blebs and biofilms that showed unique transcriptomes, profoundly distinct from spirochetes and round bodies. To better characterize differentially expressed genes in non-spirochete morphotypes, we performed functional, positional, and evolutionary enrichment analyses. Our results suggest that spirochete to round body transition relies on the delicate regulation of a relatively small number of highly conserved genes, which are located on the main chromosome and involved in translation. In contrast, spirochete to bleb or biofilm transition includes substantial reshaping of transcription profiles towards plasmids-residing and evolutionary young genes, which originated in the ancestor of Borreliaceae. Despite their abundance the function of these Borreliaceae-specific genes is largely unknown. However, many known Lyme disease virulence genes implicated in immune evasion and tissue adhesion originated in this evolutionary period. Taken together, these regularities point to the possibility that bleb and biofilm morphotypes might be important in the dissemination and persistence of B. burgdorferi inside the mammalian host. On the other hand, they prioritize the large pool of unstudied Borreliaceae-specific genes for functional characterization because this subset likely contains undiscovered Lyme disease pathogenesis genes.

Item Type: Article
Uncontrolled Keywords: transcriptomes ; Borreliella ; Borrelia ; morphotypes ; RNAseq ; evolution ; pleomorphic variants ; phylostratigraphy ; orphan genes
Subjects: NATURAL SCIENCES > Biology
NATURAL SCIENCES > Interdisciplinary Natural Sciences
Divisions: Division of Molecular Biology
Project titleProject leaderProject codeProject type
Filostratigrafija nastanka i gubitka genaDomazet-Lošo, TomislavIP-2016-06-5924HRZZ
Napredne metode i tehnologije u znanosti o podatcima i kooperativnim sustavimaUNSPECIFIEDUNSPECIFIEDEK
Inovativne strategije protiv bakterijskih infekcijaDomazet-Lošo, Tomislav955626EK
Depositing User: Nina Čorak
Date Deposited: 20 Jun 2023 13:31
DOI: 10.3390/ijms24065594

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