The Chimeric Genome of <italic toggle="yes">Sphaerochaeta</italic>: Nonspiral Spirochetes That Break with the Prevalent Dogma in Spirochete Biology

ABSTRACT Spirochaetes is one of a few bacterial phyla that are characterized by a unifying diagnostic feature, namely, the helical morphology and motility conferred by axial periplasmic flagella. Their unique morphology and mode of propulsion also represent major pathogenicity factors of clinical sp...

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Autores principales:	A. Caro-Quintero, K. M. Ritalahti, K. D. Cusick, F. E. Löffler, K. T. Konstantinidis
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2012
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d47d70a09bea4e75817f24f7b556a62d
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spelling	oai:doaj.org-article:d47d70a09bea4e75817f24f7b556a62d2021-11-15T15:39:02ZThe Chimeric Genome of <italic toggle="yes">Sphaerochaeta</italic>: Nonspiral Spirochetes That Break with the Prevalent Dogma in Spirochete Biology10.1128/mBio.00025-122150-7511https://doaj.org/article/d47d70a09bea4e75817f24f7b556a62d2012-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00025-12https://doaj.org/toc/2150-7511ABSTRACT Spirochaetes is one of a few bacterial phyla that are characterized by a unifying diagnostic feature, namely, the helical morphology and motility conferred by axial periplasmic flagella. Their unique morphology and mode of propulsion also represent major pathogenicity factors of clinical spirochetes. Here we describe the genome sequences of two coccoid isolates of the recently described genus Sphaerochaeta which are members of the phylum Spirochaetes based on 16S rRNA gene and whole-genome phylogenies. Interestingly, the Sphaerochaeta genomes completely lack the motility and associated signal transduction genes present in all sequenced spirochete genomes. Additional analyses revealed that the lack of flagella is associated with a unique, nonrigid cell wall structure hallmarked by a lack of transpeptidase and transglycosylase genes, which is also unprecedented in spirochetes. The Sphaerochaeta genomes are highly enriched in fermentation and carbohydrate metabolism genes relative to other spirochetes, indicating a fermentative lifestyle. Remarkably, most of the enriched genes appear to have been acquired from nonspirochetes, particularly clostridia, in several massive horizontal gene transfer events (>40% of the total number of genes in each genome). Such a high level of direct interphylum genetic exchange is extremely rare among mesophilic organisms and has important implications for the assembly of the prokaryotic tree of life. IMPORTANCE Spiral shape and motility historically have been the unifying hallmarks of the phylum Spirochaetes. These features also represent important virulence factors of highly invasive pathogenic spirochetes such as the causative agents of syphilis and Lyme disease. Through the integration of genome sequencing, microscopy, and physiological studies, we conclusively show that the spiral morphology and motility of spirochetes are not universal morphological properties. In particular, we found that the genomes of the members of the recently described genus Sphaerochaeta lack the genes encoding the characteristic flagellar apparatus and, in contrast to most other spirochetes, have acquired many metabolic and fermentation genes from clostridia. These findings have major implications for the isolation and study of spirochetes, the diagnosis of spirochete-caused diseases, and the reconstruction of the evolutionary history of this important bacterial phylum. The Sphaerochaeta sp. genomes offer new avenues to link ecophysiology with the functionality and evolution of the spirochete flagellar apparatus.A. Caro-QuinteroK. M. RitalahtiK. D. CusickF. E. LöfflerK. T. KonstantinidisAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 3, Iss 3 (2012)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 A. Caro-Quintero K. M. Ritalahti K. D. Cusick F. E. Löffler K. T. Konstantinidis The Chimeric Genome of <italic toggle="yes">Sphaerochaeta</italic>: Nonspiral Spirochetes That Break with the Prevalent Dogma in Spirochete Biology
description	ABSTRACT Spirochaetes is one of a few bacterial phyla that are characterized by a unifying diagnostic feature, namely, the helical morphology and motility conferred by axial periplasmic flagella. Their unique morphology and mode of propulsion also represent major pathogenicity factors of clinical spirochetes. Here we describe the genome sequences of two coccoid isolates of the recently described genus Sphaerochaeta which are members of the phylum Spirochaetes based on 16S rRNA gene and whole-genome phylogenies. Interestingly, the Sphaerochaeta genomes completely lack the motility and associated signal transduction genes present in all sequenced spirochete genomes. Additional analyses revealed that the lack of flagella is associated with a unique, nonrigid cell wall structure hallmarked by a lack of transpeptidase and transglycosylase genes, which is also unprecedented in spirochetes. The Sphaerochaeta genomes are highly enriched in fermentation and carbohydrate metabolism genes relative to other spirochetes, indicating a fermentative lifestyle. Remarkably, most of the enriched genes appear to have been acquired from nonspirochetes, particularly clostridia, in several massive horizontal gene transfer events (>40% of the total number of genes in each genome). Such a high level of direct interphylum genetic exchange is extremely rare among mesophilic organisms and has important implications for the assembly of the prokaryotic tree of life. IMPORTANCE Spiral shape and motility historically have been the unifying hallmarks of the phylum Spirochaetes. These features also represent important virulence factors of highly invasive pathogenic spirochetes such as the causative agents of syphilis and Lyme disease. Through the integration of genome sequencing, microscopy, and physiological studies, we conclusively show that the spiral morphology and motility of spirochetes are not universal morphological properties. In particular, we found that the genomes of the members of the recently described genus Sphaerochaeta lack the genes encoding the characteristic flagellar apparatus and, in contrast to most other spirochetes, have acquired many metabolic and fermentation genes from clostridia. These findings have major implications for the isolation and study of spirochetes, the diagnosis of spirochete-caused diseases, and the reconstruction of the evolutionary history of this important bacterial phylum. The Sphaerochaeta sp. genomes offer new avenues to link ecophysiology with the functionality and evolution of the spirochete flagellar apparatus.
format	article
author	A. Caro-Quintero K. M. Ritalahti K. D. Cusick F. E. Löffler K. T. Konstantinidis
author_facet	A. Caro-Quintero K. M. Ritalahti K. D. Cusick F. E. Löffler K. T. Konstantinidis
author_sort	A. Caro-Quintero
title	The Chimeric Genome of <italic toggle="yes">Sphaerochaeta</italic>: Nonspiral Spirochetes That Break with the Prevalent Dogma in Spirochete Biology
title_short	The Chimeric Genome of <italic toggle="yes">Sphaerochaeta</italic>: Nonspiral Spirochetes That Break with the Prevalent Dogma in Spirochete Biology
title_full	The Chimeric Genome of <italic toggle="yes">Sphaerochaeta</italic>: Nonspiral Spirochetes That Break with the Prevalent Dogma in Spirochete Biology
title_fullStr	The Chimeric Genome of <italic toggle="yes">Sphaerochaeta</italic>: Nonspiral Spirochetes That Break with the Prevalent Dogma in Spirochete Biology
title_full_unstemmed	The Chimeric Genome of <italic toggle="yes">Sphaerochaeta</italic>: Nonspiral Spirochetes That Break with the Prevalent Dogma in Spirochete Biology
title_sort	chimeric genome of <italic toggle="yes">sphaerochaeta</italic>: nonspiral spirochetes that break with the prevalent dogma in spirochete biology
publisher	American Society for Microbiology
publishDate	2012
url	https://doaj.org/article/d47d70a09bea4e75817f24f7b556a62d
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The Chimeric Genome of <italic toggle="yes">Sphaerochaeta</italic>: Nonspiral Spirochetes That Break with the Prevalent Dogma in Spirochete Biology

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