scholarly journals Horizontal transfer of microbial toxin genes to gall midge genomes

Author(s):  
Verster Kirsten I ◽  
Rebecca L Tarnopol ◽  
Saron M Akalu ◽  
Noah K Whiteman

Abstract A growing body of evidence has underscored the role of horizontal gene transfer (HGT) in animal evolution. Previously, we discovered the horizontal transfer of the gene encoding the eukaryotic genotoxin cytolethal distending toxin B (cdtB) from the pea aphid Acyrthosiphon pisum secondary endosymbiont (APSE) phages to drosophilid and aphid nuclear genomes. Here, we report cdtB in the nuclear genome of the gall-forming ‘swede midge’ Contarinia nasturtii (Diptera: Cecidomyiidae) via HGT. We searched all available gall midge genome sequences for evidence of APSE-to-insect HGT events and found five toxin genes (aip56, cdtB, lysozyme, rhs, and sltxB) transferred horizontally to cecidomyiid nuclear genomes. Surprisingly, phylogenetic analyses of HGT candidates indicated APSE phages were often not the ancestral donor lineage of the toxin gene to cecidomyiids. We used a phylogenetic signal statistic to test a transfer-by-proximity hypothesis for animal HGT, which suggested that microbe-to-insect HGT was more likely between taxa that share environments than those from different environments. Many of the toxins we found in midge genomes target eukaryotic cells, and catalytic residues important for toxin function are conserved in insect copies. This class of horizontally transferred, eukaryotic cell-targeting genes is potentially important in insect adaptation.

2021 ◽  
Author(s):  
Kirsten I. Verster ◽  
Rebecca L. Tarnopol ◽  
Saron M. Akalu ◽  
Noah K. Whiteman

AbstractA growing body of evidence points to a role for horizontal gene transfer (HGT) in the evolution of animal novelties. Previously, we discovered the horizontal transfer of the gene encoding the eukaryotic genotoxin cytolethal distending toxin B (CdtB) from the Acyrthosiphon pisum Secondary Endosymbiont (APSE) bacteriophage to drosophilid and aphid genomes. Here, we report that cdtB is also found in the nuclear genome of the gall-forming ‘swede midge’ Contarinia nasturtii (Diptera: Cecidomyiidae). We subsequently searched genome sequences of all available cecidomyiid species for evidence of microbe-to-insect HGT events. We found evidence of pervasive transfer of APSE-like toxin genes to cecidomyiid nuclear genomes. Many of the toxins encoded by these horizontally transferred genes target eukaryotic cells, rather than prokaryotes. In insects, catalytic residues important for toxin function are conserved. Phylogenetic analyses of HGT candidates indicated APSE phages were often not the ancestral donor of the toxin gene to cecidomyiid genomes, suggesting a broader pool of microbial donor lineages. We used a phylogenetic signal statistic to test a transfer-by-proximity hypothesis for HGT, which showed, that prokaryotic-to-insect HGT was more likely to occur between taxa in common environments. Our study highlights the horizontal transfer of genes encoding a new functional class of proteins in insects, toxins that target eukaryotic cells, which is potentially important in mediating interactions with eukaryotic pathogens and parasites.Significance StatementThe diversity of genes encoded by phages infecting bacterial symbionts of eukaryotes represents an enormous, relatively unexplored pool of new eukaryotic genes through horizontal gene transfer (HGT). In this study, we discovered pervasive HGT of toxin genes encoded by Acyrthosiphon pisum secondary endosymbiont (APSE) bacteriophages and other microbes to the nuclear genomes of gall midges (Diptera: Cecidomyiidae). We found five toxin genes were transferred horizontally from phage, bacteria, or fungi into genomes of several cecidomyiid species. These genes were aip56, cdtB, lysozyme, rhs, and sltxB. Most of the toxins encoded by these genes antagonize eukaryotic cells, and we posit that they may play a protective role in the insect immune system.


Insects ◽  
2021 ◽  
Vol 12 (5) ◽  
pp. 396
Author(s):  
Natrada Mitpuangchon ◽  
Kwan Nualcharoen ◽  
Singtoe Boonrotpong ◽  
Patamarerk Engsontia

Many animal species can produce venom for defense, predation, and competition. The venom usually contains diverse peptide and protein toxins, including neurotoxins, proteolytic enzymes, protease inhibitors, and allergens. Some drugs for cancer, neurological disorders, and analgesics were developed based on animal toxin structures and functions. Several caterpillar species possess venoms that cause varying effects on humans both locally and systemically. However, toxins from only a few species have been investigated, limiting the full understanding of the Lepidoptera toxin diversity and evolution. We used the RNA-seq technique to identify toxin genes from the stinging nettle caterpillar, Parasa lepida (Cramer, 1799). We constructed a transcriptome from caterpillar urticating hairs and reported 34,968 unique transcripts. Using our toxin gene annotation pipeline, we identified 168 candidate toxin genes, including protease inhibitors, proteolytic enzymes, and allergens. The 21 P. lepida novel Knottin-like peptides, which do not show sequence similarity to any known peptide, have predicted 3D structures similar to tarantula, scorpion, and cone snail neurotoxins. We highlighted the importance of convergent evolution in the Lepidoptera toxin evolution and the possible mechanisms. This study opens a new path to understanding the hidden diversity of Lepidoptera toxins, which could be a fruitful source for developing new drugs.


mBio ◽  
2019 ◽  
Vol 10 (2) ◽  
Author(s):  
Adrianne N. Edwards ◽  
Brandon R. Anjuwon-Foster ◽  
Shonna M. McBride

ABSTRACTClostridioides difficileinfection (CDI) is a toxin-mediated diarrheal disease. Several factors have been identified that influence the production of the two majorC. difficiletoxins, TcdA and TcdB, but prior published evidence suggested that additional unknown factors were involved in toxin regulation. Previously, we identified aC. difficileregulator, RstA, that promotes sporulation and represses motility and toxin production. We observed that the predicted DNA-binding domain of RstA was required for RstA-dependent repression of toxin genes, motility genes, andrstAtranscription. In this study, we further investigated the regulation of toxin and motility gene expression by RstA. DNA pulldown assays confirmed that RstA directly binds therstApromoter via the predicted DNA-binding domain. Through mutational analysis of therstApromoter, we identified several nucleotides that are important for RstA-dependent transcriptional regulation. Further, we observed that RstA directly binds and regulates the promoters of the toxin genestcdAandtcdB, as well as the promoters for thesigDandtcdRgenes, which encode regulators of toxin gene expression. Complementation analyses with theClostridium perfringensRstA ortholog and a multispecies chimeric RstA protein revealed that theC. difficileC-terminal domain is required for RstA DNA-binding activity, suggesting that species-specific signaling controls RstA function. Our data demonstrate that RstA is a transcriptional repressor that autoregulates its own expression and directly inhibits transcription of the two toxin genes and two positive toxin regulators, thereby acting at multiple regulatory points to control toxin production.IMPORTANCEClostridioides difficileis an anaerobic, gastrointestinal pathogen of humans and other mammals.C. difficileproduces two major toxins, TcdA and TcdB, which cause the symptoms of the disease, and forms dormant endospores to survive the aerobic environment outside the host. A recently discovered regulatory factor, RstA, inhibits toxin production and positively influences spore formation. Herein, we determine that RstA directly binds its own promoter DNA to repress its own gene transcription. In addition, our data demonstrate that RstA directly represses toxin gene expression and gene expression of two toxin gene activators, TcdR and SigD, creating a complex regulatory network to tightly control toxin production. This study provides a novel regulatory link betweenC. difficilesporulation and toxin production. Further, our data suggest thatC. difficiletoxin production is regulated through a direct, species-specific sensing mechanism.


2019 ◽  
Vol 20 (20) ◽  
pp. 5167 ◽  
Author(s):  
Qiang Li ◽  
Yuanhang Ren ◽  
Xiaodong Shi ◽  
Lianxin Peng ◽  
Jianglin Zhao ◽  
...  

In the present study, we assembled and compared two mitogenomes from the Rhizopogon genus. The two mitogenomes of R. salebrosus and R. vinicolor comprised circular DNA molecules, with the sizes of 66,704 bp and 77,109 bp, respectively. Comparative mitogenome analysis indicated that the length and base composition of protein coding genes (PCGs), rRNA genes and tRNA genes varied between the two species. Large fragments aligned between the mitochondrial and nuclear genomes of both R. salebrosus (43.41 kb) and R. vinicolor (12.83 kb) indicated that genetic transfer between mitochondrial and nuclear genomes has occurred over evolutionary time of Rhizopogon species. Intronic regions were found to be the main factors contributing to mitogenome expansion in R. vinicolor. Variations in the number and type of introns in the two mitogenomes indicated that frequent intron loss/gain events occurred during the evolution of Rhizopogon species. Phylogenetic analyses based on Bayesian inference (BI) and Maximum likelihood (ML) methods using a combined mitochondrial gene set yielded identical and well-supported tree topologies, wherein Rhizopogon species showed close relationships with Agaricales species. This is the first study of mitogenomes within the genus Rhizopogon, and it provides a basis for understanding the evolution and differentiation of mitogenomes from the ectomycorrhizal fungal genus.


2018 ◽  
Vol 81 (4) ◽  
pp. 528-533 ◽  
Author(s):  
SUIXIA LI ◽  
PANPAN WANG ◽  
JIALIN ZHAO ◽  
LUHONG ZHOU ◽  
PENGFEI ZHANG ◽  
...  

ABSTRACTThe aim of this study was to investigate the toxin gene profile and antimicrobial resistance of Staphylococcus aureus isolates from raw chicken in the People's Republic of China. In total, 289 S. aureus isolates were characterized by antimicrobial susceptibility testing, and genes encoding enterotoxins, exfoliative toxins, Panton-Valentine leukocidin, and toxic shock syndrome toxin were revealed by PCR. Overall, 46.0% of the isolates were positive for one or more toxin genes. A high proportion of toxin genes were pvl (26.6%), followed by sej (12.5%), sea (9.0%), seh (8.3%), seb (6.9%), sec (6.9%), sed (4.8%), sei (3.1%), and see (2.4%). None of the isolates harbored seg, tsst-1, or exfoliative toxin genes. In total, 29 toxin gene profiles were obtained, and pvl (10.7%) was the most frequent genotype, followed by sea (5.9%), seb (4.8%), and sej (4.2%). Furthermore, 99.7% of the strains were resistant to at least one of the tested antimicrobial agents, and 87.2% of them displayed multidrug resistance. Resistance was most frequently observed to trimethoprim-sulfamethoxazole and erythromycin (86.2% for each), followed by tetracycline (69.9%), amoxicillin–clavulanic acid (45.0%), and ampicillin (42.6%). None of the strains were resistant to vancomycin. This study indicates that S. aureus isolates from raw chicken harbored multiple toxin genes and exhibited multiple antimicrobial resistance, which represents a potential health hazard for consumers.


2020 ◽  
Vol 37 (11) ◽  
pp. 3380-3388
Author(s):  
Stephen A Smith ◽  
Nathanael Walker-Hale ◽  
Joseph F Walker

Abstract Most phylogenetic analyses assume that a single evolutionary history underlies one gene. However, both biological processes and errors can cause intragenic conflict. The extent to which this conflict is present in empirical data sets is not well documented, but if common, could have far-reaching implications for phylogenetic analyses. We examined several large phylogenomic data sets from diverse taxa using a fast and simple method to identify well-supported intragenic conflict. We found conflict to be highly variable between data sets, from 1% to >92% of genes investigated. We analyzed four exemplar genes in detail and analyzed simulated data under several scenarios. Our results suggest that alignment error may be one major source of conflict, but other conflicts remain unexplained and may represent biological signal or other errors. Whether as part of data analysis pipelines or to explore biologically processes, analyses of within-gene phylogenetic signal should become common.


2019 ◽  
Vol 400 (3) ◽  
pp. 367-381 ◽  
Author(s):  
Kristina Straub ◽  
Mona Linde ◽  
Cosimo Kropp ◽  
Samuel Blanquart ◽  
Patrick Babinger ◽  
...  

Abstract For evolutionary studies, but also for protein engineering, ancestral sequence reconstruction (ASR) has become an indispensable tool. The first step of every ASR protocol is the preparation of a representative sequence set containing at most a few hundred recent homologs whose composition determines decisively the outcome of a reconstruction. A common approach for sequence selection consists of several rounds of manual recompilation that is driven by embedded phylogenetic analyses of the varied sequence sets. For ASR of a geranylgeranylglyceryl phosphate synthase, we additionally utilized FitSS4ASR, which replaces this time-consuming protocol with an efficient and more rational approach. FitSS4ASR applies orthogonal filters to a set of homologs to eliminate outlier sequences and those bearing only a weak phylogenetic signal. To demonstrate the usefulness of FitSS4ASR, we determined experimentally the oligomerization state of eight predecessors, which is a delicate and taxon-specific property. Corresponding ancestors deduced in a manual approach and by means of FitSS4ASR had the same dimeric or hexameric conformation; this concordance testifies to the efficiency of FitSS4ASR for sequence selection. FitSS4ASR-based results of two other ASR experiments were added to the Supporting Information. Program and documentation are available at https://gitlab.bioinf.ur.de/hek61586/FitSS4ASR.


2013 ◽  
Vol 2013 ◽  
pp. 1-11 ◽  
Author(s):  
N. Indrawattana ◽  
O. Sungkhachat ◽  
N. Sookrung ◽  
M. Chongsa-nguan ◽  
A. Tungtrongchitr ◽  
...  

Periodic monitoring ofStaphylococcus aureuscharacteristics in a locality is imperative as their drug-resistant variants cause treatment problem. In this study, antibiograms, prevalence of toxin genes (sea-see, seg-ser, seu, tsst-1, eta, etb, andetd), PFGE types, accessory gene regulator (agr) groups, and ability to form biofilm of 92S. aureusThailand clinical isolates were investigated. They were classified into 10 drug groups: groups 1–7 (56 isolates) were methicillin resistant (MRSA) and 8–10 (36 isolates) were methicillin sensitive (MSSA). One isolate did not have any toxin gene, 4 isolates carried one toxin gene (seq), and 87 isolates had two or more toxin genes. No isolate hadsee, etb, ortsst-1; six isolates hadetaoretd. Combinedseg-sei-sem-sen-seoof the highly prevalentegclocus was 26.1%. Theseb, sec, sel, seu, andetaassociated significantly with MSSA;sekwas more in MRSA. Thesek-seqassociation was 52.17% while combinedsed-sejwas not found. Twenty-three PFGE types were revealed, no association of toxin genes with PFGE types. All fouragrgroups were present;agrgroup 1 was predominant (58.70%) butagrgroup 2 strains carried more toxin genes and were more frequent toxin producers. Biofilm formation was found in 72.83% of the isolates but there was no association with antibiograms. This study provides insight information on molecular and phenotypic markers of ThailandS. aureusclinical isolates which should be useful for future active surveillance that aimed to control a spread of existing antimicrobial resistant bacteria and early recognition of a newly emerged variant.


2015 ◽  
Vol 112 (33) ◽  
pp. 10133-10138 ◽  
Author(s):  
Michael W. Gray

Comparative studies of the mitochondrial proteome have identified a conserved core of proteins descended from the α-proteobacterial endosymbiont that gave rise to the mitochondrion and was the source of the mitochondrial genome in contemporary eukaryotes. A surprising result of phylogenetic analyses is the relatively small proportion (10–20%) of the mitochondrial proteome displaying a clear α-proteobacterial ancestry. A large fraction of mitochondrial proteins typically has detectable homologs only in other eukaryotes and is presumed to represent proteins that emerged specifically within eukaryotes. A further significant fraction of the mitochondrial proteome consists of proteins with homologs in prokaryotes, but without a robust phylogenetic signal affiliating them with specific prokaryotic lineages. The presumptive evolutionary source of these proteins is quite different in contending models of mitochondrial origin.


2016 ◽  
Vol 141 (6) ◽  
pp. 623-644 ◽  
Author(s):  
Dario J. Chavez ◽  
Thomas G. Beckman ◽  
José X. Chaparro

Prunus phylogeny has been extensively studied using chloroplast DNA (cpDNA) sequences. Chloroplast DNA has a slow rate of evolution, which is beneficial to determine species relationships at a deeper level. The chloroplast-based phylogenies have a limitation due to the transfer of this organelle by interspecific hybridization. This creates difficulties when studying species relationships. Interspecific hybrids in Prunus occur naturally and have been reported, which creates a problem when using cpDNA-based phylogenies to determine species relationships. The main goal of this project was to identify nuclear gene regions that could provide an improved phylogenetic signal at the species level in Prunus. A total of 11 species in Prunus and within section Prunocerasus were used. Two peach (Prunus persica) haploids were used to test the reliability of the molecular markers developed in this project to amplify single-copy genes. A total of 33 major genes associated with vernalization response, 16 with tree architecture, and 3 with isozymes, were tested. Similarly, 41 simple sequence repeat (SSR) markers, seven cpDNA regions, and the internal transcribed spacer (ITS) region, were used. Multiple gene regions were identified and provided the greatest number of characters, greatest variability, and improved phylogenetic signal at the species level in Prunus section Prunocerasus. Out of those, trnH-psbA, PGI, MAX4, AXR1, LFY, PHYE, and VRN1 are recommended for a phylogenetic analysis with a larger number of taxa. The use of potentially informative characters (PICS) as a measure of how informative a region will be for phylogenetic analyses has been previously reported beneficial in cpDNA regions and it clearly was important in this research. This will allow selecting the region(s), which can be used in phylogenetic studies with higher number of taxa.


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