scholarly journals csrBGene Duplication Drives the Evolution of Redundant Regulatory Pathways Controlling Expression of the Major Toxic Secreted Metalloproteases inVibrio tasmaniensisLGP32

mSphere ◽  
2018 ◽  
Vol 3 (6) ◽  
Author(s):  
An Ngoc Nguyen ◽  
Elena Disconzi ◽  
Guillaume M. Charrière ◽  
Delphine Destoumieux-Garzón ◽  
Philippe Bouloc ◽  
...  

ABSTRACTCsrBs are bacterial highly conserved and multiple-copy noncoding small RNAs (sRNAs) that play major roles in cell physiology and virulence. In theVibriogenus, they are known to be regulated by the two-component system VarS/VarA. They modulate the well-characterized quorum sensing pathway controlling virulence and luminescence inVibrio choleraeandVibrio harveyi, respectively. Remarkably,Vibrio tasmaniensisLGP32, an oyster pathogen that belongs to theSplendidusclade, was found to have four copies ofcsrB, namedcsrB1-4, compared to two to three copies in otherVibriospecies. Here, we show that the extracsrB4copy results from acsrB3gene duplication, a characteristic of theSplendidusclade. Interestingly,csrBgenes are regulated in different ways inV. tasmaniensis, withcsrB1expression being independent of the VarS/VarA system. We found that a complex regulatory network involving CsrBs, quorum sensing, and the stationary-phase sigma factor σS redundantly but differentially controls the production of two secreted metalloproteases, Vsm and PrtV, the former being a major determinant of theV. tasmaniensisextracellular product toxicity. In particular, we identified a novel VarS/VarA-dependent but CsrB-independent pathway that controls positively both Vsm production and PrtV production as well asrpoSexpression. Altogether, our data show that acsrBgene duplication event inV. tasmaniensissupported the evolution of the regulatory network controlling the expression of major toxic secreted metalloproteases, thereby increasing redundancy and enabling the integration of additional input signals.IMPORTANCEThe conserved CsrB sRNAs are an example of sibling sRNAs, i.e., sRNAs which are present in multiple copies in genomes. This report illustrates how new copies arise through gene duplication events and highlights two evolutionary advantages of having such multiple copies: differential regulation of the multiple copies allows integration of different input signals into the regulatory network of which they are parts, and the high redundancy that they provide confers a strong robustness to the system.

mSystems ◽  
2019 ◽  
Vol 4 (5) ◽  
Author(s):  
Haijian Du ◽  
Wenyan Zhang ◽  
Wensi Zhang ◽  
Weijia Zhang ◽  
Hongmiao Pan ◽  
...  

ABSTRACT The evolution of microbial magnetoreception (or magnetotaxis) is of great interest in the fields of microbiology, evolutionary biology, biophysics, geomicrobiology, and geochemistry. Current genomic data from magnetotactic bacteria (MTB), the only prokaryotes known to be capable of sensing the Earth’s geomagnetic field, suggests an ancient origin of magnetotaxis in the domain Bacteria. Vertical inheritance, followed by multiple independent magnetosome gene cluster loss, is considered to be one of the major forces that drove the evolution of magnetotaxis at or above the class or phylum level, although the evolutionary trajectories at lower taxonomic ranks (e.g., within the class level) remain largely unstudied. Here we report the isolation, cultivation, and sequencing of a novel magnetotactic spirillum belonging to the genus Terasakiella (Terasakiella sp. strain SH-1) within the class Alphaproteobacteria. The complete genome sequence of Terasakiella sp. strain SH-1 revealed an unexpected duplication event of magnetosome genes within the mamAB operon, a group of genes essential for magnetosome biomineralization and magnetotaxis. Intriguingly, further comparative genomic analysis suggests that the duplication of mamAB genes is a common feature in the genomes of alphaproteobacterial MTB. Taken together, with the additional finding that gene duplication appears to have also occurred in some magnetotactic members of the Deltaproteobacteria, our results indicate that gene duplication plays an important role in the evolution of magnetotaxis in the Alphaproteobacteria and perhaps the domain Bacteria. IMPORTANCE A diversity of organisms can sense the geomagnetic field for the purpose of navigation. Magnetotactic bacteria are the most primitive magnetism-sensing organisms known thus far and represent an excellent model system for the study of the origin, evolution, and mechanism of microbial magnetoreception (or magnetotaxis). The present study is the first report focused on magnetosome gene cluster duplication in the Alphaproteobacteria, which suggests the important role of gene duplication in the evolution of magnetotaxis in the Alphaproteobacteria and perhaps the domain Bacteria. A novel scenario for the evolution of magnetotaxis in the Alphaproteobacteria is proposed and may provide new insights into evolution of magnetoreception of higher species.


PeerJ ◽  
2020 ◽  
Vol 8 ◽  
pp. e8813 ◽  
Author(s):  
Kyle T. David ◽  
Jamie R. Oaks ◽  
Kenneth M. Halanych

Background Eukaryotic genes typically form independent evolutionary lineages through either speciation or gene duplication events. Generally, gene copies resulting from speciation events (orthologs) are expected to maintain similarity over time with regard to sequence, structure and function. After a duplication event, however, resulting gene copies (paralogs) may experience a broader set of possible fates, including partial (subfunctionalization) or complete loss of function, as well as gain of new function (neofunctionalization). This assumption, known as the Ortholog Conjecture, is prevalent throughout molecular biology and notably plays an important role in many functional annotation methods. Unfortunately, studies that explicitly compare evolutionary processes between speciation and duplication events are rare and conflicting. Methods To provide an empirical assessment of ortholog/paralog evolution, we estimated ratios of nonsynonymous to synonymous substitutions (ω = dN/dS) for 251,044 lineages in 6,244 gene trees across 77 vertebrate taxa. Results Overall, we found ω to be more similar between lineages descended from speciation events (p < 0.001) than lineages descended from duplication events, providing strong support for the Ortholog Conjecture. The asymmetry in ω following duplication events appears to be largely driven by an increase along one of the paralogous lineages, while the other remains similar to the parent. This trend is commonly associated with neofunctionalization, suggesting that gene duplication is a significant mechanism for generating novel gene functions.


2015 ◽  
Vol 2015 ◽  
pp. 1-11 ◽  
Author(s):  
Tianyu Zhou ◽  
Xiping Yan ◽  
Guosong Wang ◽  
Hehe Liu ◽  
Xiang Gan ◽  
...  

Peroxisome proliferators-activated receptor (PPAR) gene family members exhibit distinct patterns of distribution in tissues and differ in functions. The purpose of this study is to investigate the evolutionary impacts on diversity functions of PPAR members and the regulatory differences on gene expression patterns. 63 homology sequences of PPAR genes from 31 species were collected and analyzed. The results showed that three isolated types of PPAR gene family may emerge from twice times of gene duplication events. The conserved domains of HOLI (ligand binding domain of hormone receptors) domain and ZnF_C4 (C4 zinc finger in nuclear in hormone receptors) are essential for keeping basic roles of PPAR gene family, and the variant domains of LCRs may be responsible for their divergence in functions. The positive selection sites in HOLI domain are benefit for PPARs to evolve towards diversity functions. The evolutionary variants in the promoter regions and 3′ UTR regions of PPARs result into differential transcription factors and miRNAs involved in regulating PPAR members, which may eventually affect their expressions and tissues distributions. These results indicate that gene duplication event, selection pressure on HOLI domain, and the variants on promoter and 3′ UTR are essential for PPARs evolution and diversity functions acquired.


mBio ◽  
2014 ◽  
Vol 5 (5) ◽  
Author(s):  
Xilan Yu ◽  
Steven P. Lund ◽  
Jessica W. Greenwald ◽  
Angela H. Records ◽  
Russell A. Scott ◽  
...  

ABSTRACTThe plant pathogenPseudomonas syringaepv. syringae B728a grows and survives on leaf surfaces and in the leaf apoplast of its host, bean (Phaseolus vulgaris). To understand the contribution of distinct regulators to B728a fitness and pathogenicity, we performed a transcriptome analysis of strain B728a and nine regulatory mutants recovered from the surfaces and interior of leaves and exposed to environmental stresses in culture. The quorum-sensing regulators AhlR and AefR influenced few genesin plantaorin vitro. In contrast, GacS and a downstream regulator, SalA, formed a large regulatory network that included a branch that regulated diverse traits and was independent of plant-specific environmental signals and a plant signal-dependent branch that positively regulated secondary metabolite genes and negatively regulated the type III secretion system. SalA functioned as a central regulator of iron status based on its reciprocal regulation of pyoverdine and achromobactin genes and also sulfur uptake, suggesting a role in the iron-sulfur balance. RetS functioned almost exclusively to repress secondary metabolite genes when the cells were not on leaves. Among the sigma factors examined, AlgU influenced many more genes than RpoS, and most AlgU-regulated genes depended on RpoN. RpoN differentially impacted many AlgU- and GacS-activated genes in cells recovered from apoplastic versus epiphytic sites, suggesting differences in environmental signals or bacterial stress status in these two habitats. Collectively, our findings illustrate a central role for GacS, SalA, RpoN, and AlgU in global regulation in B728ain plantaand a high level of plasticity in these regulators’ responses to distinct environmental signals.IMPORTANCELeaves harbor abundant microorganisms, all of which must withstand challenges such as active plant defenses and a highly dynamic environment. Some of these microbes can influence plant health. Despite knowledge of individual regulators that affect the fitness or pathogenicity of foliar pathogens, our understanding of the relative importance of various global regulators to leaf colonization is limited.Pseudomonas syringaestrain B728a is a plant pathogen and a good colonist of both the surfaces and interior of leaves. This study used global transcript profiles of strain B728a to investigate the complex regulatory network of putative quorum-sensing regulators, two-component regulators, and sigma factors in cells colonizing the leaf surface and leaf interior under stressfulin vitroconditions. The results highlighted the value of evaluating these networksin plantadue to the impact of leaf-specific environmental signals and suggested signal differences that may enable cells to differentiate surface versus interior leaf habitats.


2017 ◽  
Vol 199 (21) ◽  
Author(s):  
Jean-Paul Toussaint ◽  
Anna Farrell-Sherman ◽  
Tamar Perla Feldman ◽  
Nicole E. Smalley ◽  
Amy L. Schaefer ◽  
...  

ABSTRACT The laboratory strain of Pseudomonas aeruginosa, PAO1, activates genes for catabolism of adenosine using quorum sensing (QS). However, this strain is not well-adapted for growth on adenosine, with doubling times greater than 40 h. We previously showed that when PAO1 is grown on adenosine and casein, variants emerge that grow rapidly on adenosine. To understand the mechanism by which this adaptation occurs, we performed whole-genome sequencing of five isolates evolved for rapid growth on adenosine. All five genomes had a gene duplication-amplification (GDA) event covering several genes, including the quorum-regulated nucleoside hydrolase gene, nuh, and PA0148, encoding an adenine deaminase. In addition, two of the growth variants also exhibited a nuh promoter mutation. We recapitulated the rapid growth phenotype with a plasmid containing six genes common to all the GDA events. We also showed that nuh and PA0148, the two genes at either end of the common GDA, were sufficient to confer rapid growth on adenosine. Additionally, we demonstrated that the variant nuh promoter increased basal expression of nuh but maintained its QS regulation. Therefore, GDA in P. aeruginosa confers the ability to grow efficiently on adenosine while maintaining QS regulation of nucleoside catabolism. IMPORTANCE Pseudomonas aeruginosa thrives in many habitats and is an opportunistic pathogen of humans. In these diverse environments, P. aeruginosa must adapt to use myriad potential carbon sources. P. aeruginosa PAO1 cannot grow efficiently on nucleosides, including adenosine; however, it can acquire this ability through genetic adaptation. We show that the mechanism of adaptation is by amplification of a specific region of the genome and that the amplification preserves the regulation of the adenosine catabolic pathway by quorum sensing. These results demonstrate an underexplored mechanism of adaptation by P. aeruginosa, with implications for phenotypes such as development of antibiotic resistance.


2017 ◽  
Author(s):  
David M. Emms ◽  
Steven Kelly

AbstractThe correct interpretation of a phylogenetic tree is dependent on it being correctly rooted. A gene duplication event at the base of a clade of species is synapamorphic, and thus excludes the root of the species tree from that clade. We present STRIDE, a fast, effective, and outgroup-free method for species tree root inference from gene duplication events. STRIDE identifies sets of well-supported gene duplication events from cohorts of gene trees, and analyses these events to infer a probability distribution over an unrooted species tree for the location of the true root. We show that STRIDE infers the correct root of the species tree for a large range of simulated and real species sets. We demonstrate that the novel probability model implemented in STRIDE can accurately represent the ambiguity in species tree root assignment for datasets where information is limited. Furthermore, application of STRIDE to inference of the origin of the eukaryotic tree resulted in a root probability distribution that was consistent with, but unable to distinguish between, leading hypotheses for the origin of the eukaryotes. In summary, STRIDE is a fast, scalable, and effective method for species tree root inference from genome scale data.


2018 ◽  
Vol 84 (8) ◽  
pp. e00114-18 ◽  
Author(s):  
Lu Zhang ◽  
Yanqiang Liu ◽  
Yunpeng Yang ◽  
Weihong Jiang ◽  
Yang Gu

ABSTRACTThe master regulator CcpA (catabolite control protein A) manages a large and complex regulatory network that is essential for cellular physiology and metabolism in Gram-positive bacteria. Although CcpA can affect the expression of target genes by binding to acis-acting catabolite-responsive element (cre), whether and how the expression of CcpA is regulated remain poorly explored. Here, we report a novel dual-cremotif that is employed by the CcpA inClostridium acetobutylicum, a typical solventogenicClostridiumspecies, for autoregulation. Twocresites are involved in CcpA autoregulation, and they reside in the promoter and coding regions of CcpA. In this dual-cremotif,creP, in the promoter region, positively regulatesccpAtranscription, whereascreORF, in the coding region, negatively regulates this transcription, thus enabling two-way autoregulation of CcpA. Although CcpA boundcrePmore strongly thancreORFin vitro, thein vivoassay showed thatcreORF-based repression dominates CcpA autoregulation during the entire fermentation. Finally, a synonymous mutation ofcreORFwas made within the coding region, achieving an increased intracellular CcpA expression and improved cellular performance. This study provides new insights into the regulatory role of CcpA inC. acetobutylicumand, moreover, contributes a new engineering strategy for this industrial strain.IMPORTANCECcpA is known to be a key transcription factor in Gram-positive bacteria. However, it is still unclear whether and how the intracellular CcpA level is regulated, which may be essential for maintaining normal cell physiology and metabolism. We discovered here that CcpA employs a dual-cremotif to autoregulate, enabling dynamic control of its own expression level during the entire fermentation process. This finding answers the questions above and fills a void in our understanding of the regulatory network of CcpA. Interference in CcpA autoregulation leads to improved cellular performance, providing a new useful strategy in genetic engineering ofC. acetobutylicum. Since CcpA is widespread in Gram-positive bacteria, including pathogens, this dual-cre-based CcpA autoregulation would be valuable for increasing our understanding of CcpA-based global regulation in bacteria.


2016 ◽  
Vol 198 (12) ◽  
pp. 1725-1734
Author(s):  
Kimberly A. Walker ◽  
Lauren A. Griggs ◽  
Markus Obrist ◽  
Addys Bode ◽  
R. Patrick Summers ◽  
...  

ABSTRACTTheYersinia enterocoliticaYsa type III secretion system (T3SS) is associated with intracellular survival, and, like other characterized T3SSs, it is tightly controlled. Expression of theysagenes is only detected following growth at low temperatures (26°C) and in high concentrations of sodium chloride (290 mM) in the medium. The YsrSTR phosphorelay (PR) system is required forysaexpression and likely responds to NaCl. During our investigations into the Ysr PR system, we discovered that genes YE3578 and YE3579 are remarkably similar toysrRandysrS, respectively, and are probably a consequence of a gene duplication event. The amino acid differences between YE3578 andysrRare primarily clustered into two short regions. The differences between YE3579 andysrSare nearly all located in the periplasmic sensing domain; the cytoplasmic domains are 98% identical. We investigated whether these paralogs were capable of activatingysagene expression. We found that the sensor paralog, named DygS, is capable of compensating for loss ofysrS, but the response regulator paralog, DygR, cannot complement aysrRgene deletion. In addition, YsrR, but not DygR, interacts with the histidine phosphorelay protein YsrT. Thus, DygS likely activatesysagene expression in response to a signal other than NaCl and provides an example of a phosphorelay system in which two sensor kinases feed into the same regulatory pathway.IMPORTANCEAll organisms need mechanisms to promote survival in changing environments. Prokaryotic phosphorelay systems are minimally comprised of a histidine kinase (HK) that senses an extracellular stimulus and a response regulator (RR) but can contain three or more proteins. Through gene duplication, a unique hybrid HK was created. We show that, while the hybrid appears to retain all of the phosphorelay functions, it responds to a different signal than the original. Both HKs transmit the signal to the same RR, which activates a promoter that transcribes a set of genes encoding a type III secretion system (T3SS) whose function is not yet evident. The significance of this work lies in finding that two HKs regulate this T3SS, highlighting its importance.


2018 ◽  
Vol 200 (14) ◽  
Author(s):  
Anthony Harrington ◽  
Yftah Tal-Gan

ABSTRACTStreptococcus gallolyticussubsp.gallolyticus, a member of the group D streptococci, is normally found in the bovine rumen and human gut. It is an opportunistic pathogen that was recently determined to be a bacterial driver of colorectal cancer, in addition to causing other diseases, such as infective endocarditis, bacteremia, neonatal meningitis, and septicemia. As an emerging pathogen, not much is known about this bacterium, its virulence mechanisms, or its virulence regulatory pathways. Previous studies suggest thatS. gallolyticussubsp.gallolyticususes a ComRS pathway, one of manyStreptococcusquorum-sensing circuitries, for competence. However, thus far, the ubiquitous ComABCDE pathway has not been studied, nor has its regulatory role inS. gallolyticussubsp.gallolyticus. We therefore sought to study theS. gallolyticussubsp.gallolyticusComABCDE quorum-sensing pathway and have identified its peptide pheromone, which is termed the competence-stimulating peptide (CSP). We further determined that this peptide regulates the production of bacteriocin-like inhibitory substances (BLISs), a phenotype that has been linked with the ComABCDE pathway in bothStreptococcus pneumoniaeandStreptococcus mutans. Our data show thatS. gallolyticussubsp.gallolyticusTX20005 produces a 21-mer CSP signal, which differs from CSP signals of otherStreptococcusspecies in that its active form begins three residues after the double-glycine leader signal of the ComC precursor peptide. Additionally, our data suggest that this peptide might not be related to competence induction, as opposed to CSP signaling peptides in otherStreptococcusspecies. This study provides the first evidence thatS. gallolyticussubsp.gallolyticusutilizes quorum sensing to eliminate competitors, presenting a potential pathway to target this emerging human pathogen.IMPORTANCEStreptococcus gallolyticussubsp.gallolyticusis an emerging human pathogen known as a causative agent of infective endocarditis, and recently, of colorectal cancer. In this work, we revealed a functional quorum-sensing circuitry inS. gallolyticussubsp.gallolyticus, including the identification of the central signaling peptide pheromone, competence-stimulating peptide (CSP), and the regulatory role of this circuitry in the production of bacteriocin-like inhibitory substances (BLISs). This work uncovered a mechanism by which this bacterium outcompetes other bacterial species and thus provides a potential tool to study this opportunistic pathogen.


2021 ◽  
Vol 21 (1) ◽  
Author(s):  
Yuwei Wang ◽  
Baocheng Guo

Abstract Background Gene duplication and alternative splicing (AS) are two distinct mechanisms generating new materials for genetic innovations. The evolutionary link between gene duplication and AS is still controversial, due to utilizing duplicates from inconsistent ages of duplication events in earlier studies. With the aid of RNA-seq data, we explored evolutionary scenario of AS divergence between duplicates with ohnologs that resulted from the teleost genome duplication event in zebrafish, medaka, and stickleback. Results Ohnologs in zebrafish have fewer AS forms compared to their singleton orthologs, supporting the function-sharing model of AS divergence between duplicates. Ohnologs in stickleback have more AS forms compared to their singleton orthologs, which supports the accelerated model of AS divergence between duplicates. The evolution of AS in ohnologs in medaka supports a combined scenario of the function-sharing and the accelerated model of AS divergence between duplicates. We also found a small number of ohnolog pairs in each of the three teleosts showed significantly asymmetric AS divergence. For example, the well-known ovary-factor gene cyp19a1a has no AS form but its ohnolog cyp19a1b has multiple AS forms in medaka, suggesting that functional divergence between duplicates might have result from AS divergence. Conclusions We found that a combined scenario of function-sharing and accelerated models for AS evolution in ohnologs in teleosts and rule out the independent model that assumes a lack of correlation between gene duplication and AS. Our study thus provided insights into the link between gene duplication and AS in general and ohnolog divergence in teleosts from AS perspective in particular.


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