scholarly journals From root to tips: sporulation evolution and specialization inBacillus subtilisand the intestinal pathogenClostridioides difficile

2019 ◽  
Author(s):  
Paula Ramos-Silva ◽  
Mónica Serrano ◽  
Adriano O. Henriques

AbstractBacteria of the Firmicutes phylum are able to enter a developmental pathway that culminates with the formation of a highly resistant, dormant spore. Spores allow environmental persistence, dissemination and for pathogens, are infection vehicles. In both the modelBacillus subtilis, an aerobic species, and in the intestinal pathogenClostridioides difficile, an obligate anaerobe, sporulation mobilizes hundreds of genes. Their expression is coordinated between the forespore and the mother cell, the two cells that participate in the process, and is kept in close register with the course of morphogenesis. The evolutionary mechanisms by which sporulation emerged and evolved in these two species, and more broadly across Firmicutes, remain largely unknown. Here, we trace the origin and evolution of sporulation. Using the genes involved in the process inB. subtilisandC. difficile, and estimating their gain-loss dynamics in a comprehensive bacterial macro-evolutionary framework we show that sporulation evolution was driven by two major gene gain events, the first at the base of the Firmicutes and the second at the base of theB. subtilisgroup and within the Peptostreptococcaceae family, which includesC. difficile. We also show that early and late sporulation regulons have been co-evolving and that sporulation genes entail greater innovation inB. subtiliswith many Bacilli-lineage restricted genes. In contrast,C. difficilemore often recruits new sporulation genes by horizontal gene transfer, which reflects both its highly mobile genome, the complexity of the gut microbiota and an adjustment of sporulation to this particular ecosystem.

2019 ◽  
Vol 36 (12) ◽  
pp. 2714-2736 ◽  
Author(s):  
Paula Ramos-Silva ◽  
Mónica Serrano ◽  
Adriano O Henriques

Abstract Bacteria of the Firmicutes phylum are able to enter a developmental pathway that culminates with the formation of highly resistant, dormant endospores. Endospores allow environmental persistence, dissemination and for pathogens, are also infection vehicles. In both the model Bacillus subtilis, an aerobic organism, and in the intestinal pathogen Clostridioides difficile, an obligate anaerobe, sporulation mobilizes hundreds of genes. Their expression is coordinated between the forespore and the mother cell, the two cells that participate in the process, and is kept in close register with the course of morphogenesis. The evolutionary mechanisms by which sporulation emerged and evolved in these two species, and more broadly across Firmicutes, remain largely unknown. Here, we trace the origin and evolution of sporulation using the genes known to be involved in the process in B. subtilis and C. difficile, and estimating their gain-loss dynamics in a comprehensive bacterial macroevolutionary framework. We show that sporulation evolution was driven by two major gene gain events, the first at the base of the Firmicutes and the second at the base of the B. subtilis group and within the Peptostreptococcaceae family, which includes C. difficile. We also show that early and late sporulation regulons have been coevolving and that sporulation genes entail greater innovation in B. subtilis with many Bacilli lineage-restricted genes. In contrast, C. difficile more often recruits new sporulation genes by horizontal gene transfer, which reflects both its highly mobile genome, the complexity of the gut microbiota, and an adjustment of sporulation to the gut ecosystem.


Author(s):  
Noah Budi ◽  
Jared J. Godfrey ◽  
Nasia Safdar ◽  
Sanjay K. Shukla ◽  
Warren E. Rose

Clostridioides difficile (C. difficile) infections (CDI) are commonly treated with antibiotics that do not impact the dormant spore form of the pathogen. CDI-directed antibiotics, such as vancomycin and metronidazole, can destroy the vegetative form of C. difficile and protective microbiota. After treatment, spores can germinate into vegetative cells causing clinical disease relapse and further spore shedding. This in vitro study compares the combination of germinants with vancomycin or omadacycline to antibiotics alone in eradicating C. difficile spores and vegetative cells. Among the four strains in this study, omadacycline minimum inhibitory concentrations (0.031-0.125 mg/L) were lower than vancomycin (1-4 mg/L). Omadacycline nor vancomycin in media alone reduced spore counts. In three of the four strains, including the epidemic ribotype 027, spore eradication with germinants was 94.8-97.4% with vancomycin and 99.4-99.8% with omadacycline (p<0.005). In ribotype 012, either antibiotic combined with germinants resulted in 100% spore eradication at 24 hours. The addition of germinants with either antibiotic did not result in significant toxin A or B production, which were below the limit of detection (<1.25 ng/mL) by 48 hours. Limiting the number of spores present in patient GI tracts at the end of therapy may be effective at preventing recurrent CDI and limiting spore shedding in the healthcare environment. These results with germinants warrant safety and efficacy evaluations in animal models.


2020 ◽  
Vol 38 (1) ◽  
pp. 2-15 ◽  
Author(s):  
Julien Martinez ◽  
Lisa Klasson ◽  
John J Welch ◽  
Francis M Jiggins

Abstract Cytoplasmic incompatibility is a selfish reproductive manipulation induced by the endosymbiont Wolbachia in arthropods. In males Wolbachia modifies sperm, leading to embryonic mortality in crosses with Wolbachia-free females. In females, Wolbachia rescues the cross and allows development to proceed normally. This provides a reproductive advantage to infected females, allowing the maternally transmitted symbiont to spread rapidly through host populations. We identified homologs of the genes underlying this phenotype, cifA and cifB, in 52 of 71 new and published Wolbachia genome sequences. They are strongly associated with cytoplasmic incompatibility. There are up to seven copies of the genes in each genome, and phylogenetic analysis shows that Wolbachia frequently acquires new copies due to pervasive horizontal transfer between strains. In many cases, the genes have subsequently acquired loss-of-function mutations to become pseudogenes. As predicted by theory, this tends to occur first in cifB, whose sole function is to modify sperm, and then in cifA, which is required to rescue the cross in females. Although cif genes recombine, recombination is largely restricted to closely related homologs. This is predicted under a model of coevolution between sperm modification and embryonic rescue, where recombination between distantly related pairs of genes would create a self-incompatible strain. Together, these patterns of gene gain, loss, and recombination support evolutionary models of cytoplasmic incompatibility.


2020 ◽  
Vol 8 (11) ◽  
pp. 1739
Author(s):  
David E. Whitworth ◽  
Allison Zwarycz

As prokaryotes diverge by evolution, essential ‘core’ genes required for conserved phenotypes are preferentially retained, while inessential ‘accessory’ genes are lost or diversify. We used the recently expanded number of myxobacterial genome sequences to investigate the conservation of their signalling proteins, focusing on two sister genera (Myxococcus and Corallococcus), and on a species within each genus (Myxococcus xanthus and Corallococcus exiguus). Four new C. exiguus genome sequences are also described here. Despite accessory genes accounting for substantial proportions of each myxobacterial genome, signalling proteins were found to be enriched in the core genome, with two-component system genes almost exclusively so. We also investigated the conservation of signalling proteins in three myxobacterial behaviours. The linear carotenogenesis pathway was entirely conserved, with no gene gain/loss observed. However, the modular fruiting body formation network was found to be evolutionarily plastic, with dispensable components in all modules (including components required for fruiting in the model myxobacterium M. xanthus DK1622). Quorum signalling (QS) is thought to be absent from most myxobacteria, however, they generally appear to be able to produce CAI-I (cholerae autoinducer-1), to sense other QS molecules, and to disrupt the QS of other organisms, potentially important abilities during predation of other prokaryotes.


PLoS ONE ◽  
2010 ◽  
Vol 5 (6) ◽  
pp. e11147 ◽  
Author(s):  
Aaron E. Darling ◽  
Bob Mau ◽  
Nicole T. Perna

PLoS ONE ◽  
2021 ◽  
Vol 16 (3) ◽  
pp. e0246651
Author(s):  
Lizeth Soto-Avila ◽  
Ricardo Ciria Merce ◽  
Walter Santos ◽  
Nori Castañeda ◽  
Rosa-María Gutierrez-Ríos

Engulfment requires the coordinated, targeted synthesis and degradation of peptidoglycan at the leading edge of the engulfing membrane to allow the mother cell to completely engulf the forespore. Proteins such as the DMP and Q:AH complexes in Bacillus subtilis are essential for engulfment, as are a set of accessory proteins including GerM and SpoIIB, among others. Experimental and bioinformatic studies of these proteins in bacteria distinct from Bacillus subtilis indicate that fundamental differences exist regarding the organization and mechanisms used to successfully perform engulfment. As a consequence, the distribution and prevalence of the proteins involved in engulfment and other proteins that participate in different sporulation stages have been studied using bioinformatic approaches. These works are based on the prediction of orthologs in the genomes of representative Firmicutes and have been helpful in tracing hypotheses about the origin and evolution of sporulation genes, some of which have been postulated as sporulation signatures. To date, an extensive study of these signatures outside of the representative Firmicutes is not available. Here, we asked whether phyletic profiles of proteins involved in engulfment can be used as signatures able to describe the sporulation phenotype. We tested this hypothesis in a set of 954 Firmicutes, finding preserved phyletic profiles defining signatures at the genus level. Finally, a phylogenetic reconstruction based on non-redundant phyletic profiles at the family level shows the non-monophyletic origin of these proteins due to gain/loss events along the phylum Firmicutes.


2021 ◽  
Vol 12 ◽  
Author(s):  
Rachana Banerjee ◽  
Narendrakumar M. Chaudhari ◽  
Abhishake Lahiri ◽  
Anupam Gautam ◽  
Debaleena Bhowmik ◽  
...  

Sulfolobaceae family, comprising diverse thermoacidophilic and aerobic sulfur-metabolizing Archaea from various geographical locations, offers an ideal opportunity to infer the evolutionary dynamics across the members of this family. Comparative pan-genomics coupled with evolutionary analyses has revealed asymmetric genome evolution within the Sulfolobaceae family. The trend of genome streamlining followed by periods of differential gene gains resulted in an overall genome expansion in some species of this family, whereas there was reduction in others. Among the core genes, both Sulfolobus islandicus and Saccharolobus solfataricus showed a considerable fraction of positively selected genes and also higher frequencies of gene acquisition. In contrast, Sulfolobus acidocaldarius genomes experienced substantial amount of gene loss and strong purifying selection as manifested by relatively lower genome size and higher genome conservation. Central carbohydrate metabolism and sulfur metabolism coevolved with the genome diversification pattern of this archaeal family. The autotrophic CO2 fixation with three significant positively selected enzymes from S. islandicus and S. solfataricus was found to be more imperative than heterotrophic CO2 fixation for Sulfolobaceae. Overall, our analysis provides an insight into the interplay of various genomic adaptation strategies including gene gain–loss, mutation, and selection influencing genome diversification of Sulfolobaceae at various taxonomic levels and geographical locations.


2016 ◽  
Author(s):  
Pavel Avdeyev ◽  
Shuai Jiang ◽  
Sergey Aganezov ◽  
Fei Hu ◽  
Max A. Alekseyev

Since most dramatic genomic changes are caused by genome rearrangements as well as gene duplications and gain/loss events, it becomes crucial to understand their mechanisms and reconstruct ancestral genomes of the given genomes. This problem was shown to be NP-complete even in the "simplest" case of three genomes, thus calling for heuristic rather than exact algorithmic solutions. At the same time, a larger number of input genomes may actually simplify the problem in practice as it was earlier illustrated with MGRA, a state-of-the-art software tool for reconstruction of ancestral genomes of multiple genomes. One of the key obstacles for MGRA and other similar tools is presence of breakpoint reuses when the same breakpoint region is broken by several different genome rearrangements in the course of evolution. Furthermore, such tools are often limited to genomes composed of the same genes with each gene present in a single copy in every genome. This limitation makes these tools inapplicable for many biological datasets and degrades the resolution of ancestral reconstructions in diverse datasets. We address these deficiencies by extending the MGRA algorithm to genomes with unequal gene contents. The developed next-generation tool MGRA2 can handle gene gain/loss events and shares the ability of MGRA to reconstruct ancestral genomes uniquely in the case of limited breakpoint reuse. Furthermore, MGRA2 employs a number of novel heuristics to cope with higher breakpoint reuse and process datasets inaccessible for MGRA. In practical experiments, MGRA2 shows superior performance for simulated and real genomes as compared to other ancestral genomes reconstruction tools. The MGRA2 tool is distributed as an open-source software and can be downloaded from GitHub repository http://github.com/ablab/mgra/. It is also available in the form of a web-server at http://mgra.cblab.org, which makes it readily accessible for inexperienced users.


2021 ◽  
Author(s):  
Yisong Li ◽  
Zhong-Zhi Sun ◽  
Jin-Cheng Rong ◽  
Bin-Bin Xie

Abstract Background: Micrococcus luteus is a group of actinobacteria that is widely used in biotechnology and is being thought as an emerging nosocomial pathogen. With one of the smallest genomes of free-living actinobacteria, it is found in a wide range of environments, but intraspecies genetic diversity and adaptation strategies to various environments remain unclear. Here, comparative genomics, phylogenomics, and genome-wide association studies were used to investigate the genomic diversity, evolutionary history, and the potential ecological differentiation of the species.Results: High-quality genomes of 66 M. luteus strains were downloaded from the NCBI GenBank database and core and pan-genome analysis revealed a considerable intraspecies heterogeneity. Phylogenomic analysis, gene content comparison, and average nucleotide identity calculation consistently indicated that the species has diverged into three well-differentiated clades. Population structure analysis further suggested the existence of an unknown ancestor or the fourth, yet unsampled, clade. Reconstruction of gene gain/loss events along the evolutionary history revealed both early events that contributed to the inter-clade divergence and recent events leading to the intra-clade diversity. We also found convincing evidence that recombination has played a key role of the evolutionary process of the species, with upto two-thirds of the core genes have been affected by recombination. Furthermore, distribution of mammal-associated strains (including pathogens) on the phylogenetic tree suggested that the last common ancestor had a free-living lifestyle, and a few recently diverged lineages have developed a mammal-associated lifestyle separately. Consistently, genome-wide association analysis revealed that mammal-associated strains from different lineages shared genes functionally relevant to the host-associated lifestyle, indicating a recent ecological adaption to the new host-associated habitats.Conclusions: These results revealed high intraspecies genomic diversity of M. luteus and highlighted that gene gain/loss events and extensive recombination events played key roles in the genome evolution. Our study also indicated that, as a free-living species, some lineages have recently developed or are developing a mammal-associated lifestyle. This study provides insights into the mechanisms that drive the genome evolution and adaption to various environments of a bacterial species.


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