scholarly journals Gene Transfer Agents in Plant Pathogenic Bacteria: Comparative Mobilomics, Genomic Survey and Recombinogenic Impacts

2019 ◽  
Author(s):  
Mustafa O. Jibrin ◽  
Gerald V. Minsavage ◽  
Erica M. Goss ◽  
Pamela D. Roberts ◽  
Jeffrey B. Jones

AbstractBackgroundGene transfer agents (GTAs) are phage-like mediators of gene transfer in bacterial species. Typically, strains of a bacteria species which have GTA shows more recombination than strains without GTAs. GTA-mediated gene transfer activity has been shown for few bacteria, with Rhodobacter capsulatus being the prototypical GTA. GTA have not been previously studied in plant pathogenic bacteria. A recent study inferring recombination in strains of the bacterial spot xanthomonads identified a Nigerian lineage which showed unusual recombination background. We initially set out to understand genomic drivers of recombination in this genome by focusing on mobile genetic elements.ResultsWe identified a unique cluster which was present in the Nigerian strain but absent in other sequenced strains of bacterial spot xanthomonads. The protein sequence of a gene within this cluster contained the GTA_TIM domain that is present in bacteria with GTA. We identified GTA clusters in other Xanthomonas species as well as species of Agrobacterium and Pantoea. Recombination analyses showed that generally, strains of Xanthomonas with GTA have more inferred recombination events than strains without GTA, which could lead to genome divergence.ConclusionThis study identified GTA clusters in species of the plant pathogen genera Xanthomonas, Agrobacterium and Pantoea which we have named XpGTA, AgGTA and PaGTA respectively. Our recombination analyses suggest that Xanthomonas strains with GTA generally have more inferred recombination events than strains without GTA. The study is important in understanding the drivers of evolution of bacterial plant pathogens.

2019 ◽  
Author(s):  
Mustafa O Jibrin ◽  
Gerald V. Minsavage ◽  
Erica M. Goss ◽  
Pamela D. Roberts ◽  
Jeffrey B Jones

Abstract Background Gene transfer agents (GTAs) are phage-like mediators of gene transfer in bacterial species. Typically, strains of a bacteria species which have GTA shows more recombination than strains without GTAs. GTA-mediated gene transfer activity has been shown for few bacteria, with Rhodobacter capsulatus being the prototypical GTA. GTA have not been previously studied in plant pathogenic bacteria. A recent study inferring recombination in strains of the bacterial spot xanthomonads identified a Nigerian lineage which showed unusual recombination background. We initially set out to understand genomic drivers of recombination in this genome by focusing on mobile genetic elements. Results We identified a unique cluster which was present in the Nigerian strain but absent in other sequenced strains of bacterial spot xanthomonads. The protein sequence of a gene within this cluster contained the GTA_TIM domain that is present in bacteria with GTA. We identified GTA clusters in other Xanthomonas species as well as species of Agrobacterium and Pantoea. Recombination analyses showed that generally, strains of Xanthomonas with GTA have more inferred recombination events than strains without GTA, which could lead to genome divergence.Conclusion This study identified GTA clusters in species of the plant pathogen genera Xanthomonas, Agrobacterium and Pantoea which we have named XpGTA, AgGTA and PaGTA respectively. Our recombination analyses suggest that Xanthomonas strains with GTA generally have more inferred recombination events than strains without GTA. The study is important in understanding the drivers of evolution of bacterial plant pathogens.


Insects ◽  
2022 ◽  
Vol 13 (1) ◽  
pp. 86
Author(s):  
Xiaohui Yang ◽  
Yu Hui ◽  
Daohong Zhu ◽  
Yang Zeng ◽  
Lvquan Zhao ◽  
...  

Dryocosmus kuriphilus (Hymenoptera: Cynipidae) induces galls on chestnut trees, which results in massive yield losses worldwide. Torymus sinensis (Hymenoptera: Torymidae) is a host-specific parasitoid that phenologically synchronizes with D. kuriphilus. Bacteria play important roles in the life cycle of galling insects. The aim of this research is to investigate the bacterial communities and predominant bacteria of D. kuriphilus, T. sinensis, D. kuriphilus galls and the galled twigs of Castanea mollissima. We sequenced the V5–V7 region of the bacterial 16S ribosomal RNA in D. kuriphilus, T. sinensis, D. kuriphilus galls and galled twigs using high-throughput sequencing for the first time. We provide the first evidence that D. kuriphilus shares most bacterial species with T. sinensis, D. kuriphilus galls and galled twigs. The predominant bacteria of D. kuriphilus are Serratia sp. and Pseudomonas sp. Furthermore, the bacterial community structures of D. kuriphilus and T. sinensis clearly differ from those of the other groups. Many species of the Serratia and Pseudomonas genera are plant pathogenic bacteria, and we suggest that D. kuriphilus may be a potential vector of plant pathogens. Furthermore, a total of 111 bacteria are common to D. kuriphilus adults, T. sinensis, D. kuriphilus galls and galled twigs, and we suggest that the bacteria may transmit horizontally among D. kuriphilus, T. sinensis, D. kuriphilus galls and galled twigs on the basis of their ecological associations.


Author(s):  
Emma Esterman ◽  
Yuri I. Wolf ◽  
Roman Kogay ◽  
Eugene V. Koonin ◽  
Olga Zhaxybayeva

AbstractGene transfer agents (GTAs) are virus-like particles encoded and produced by many bacteria and archaea. Unlike viruses, GTAs package fragments of the host genome instead of the genes that encode the components of the GTA itself. As a result of this non-specific DNA packaging, GTAs can transfer genes within bacterial and archaeal communities. GTAs clearly evolved from viruses and are thought to have been maintained in prokaryotic genomes due to the advantages associated with their DNA transfer capacity. The most-studied GTA is produced by the alphaproteobacterium Rhodobacter capsulatus (RcGTA), which packages random portions of the host genome at a lower DNA density than usually observed in tailed bacterial viruses. How the DNA packaging properties of RcGTA evolved from those of the ancestral virus remains unknown. To address this question, we reconstructed the evolutionary history of the large subunit of the terminase (TerL), a highly conserved enzyme used by viruses and GTAs to package DNA. We found that RcGTA-like TerLs grouped within viruses that employ the headful packaging strategy. Because distinct mechanisms of viral DNA packaging correspond to differences in the TerL amino acid sequence, our finding suggests that RcGTA evolved from a headful packaging virus. Headful packaging is the least sequence-specific mode of DNA packaging, which would facilitate the switch from packaging of the viral genome to packaging random pieces of the host genome during GTA evolution.


2019 ◽  
Vol 11 (10) ◽  
pp. 2941-2953 ◽  
Author(s):  
Roman Kogay ◽  
Taylor B Neely ◽  
Daniel P Birnbaum ◽  
Camille R Hankel ◽  
Migun Shakya ◽  
...  

Abstract Many of the sequenced bacterial and archaeal genomes encode regions of viral provenance. Yet, not all of these regions encode bona fide viruses. Gene transfer agents (GTAs) are thought to be former viruses that are now maintained in genomes of some bacteria and archaea and are hypothesized to enable exchange of DNA within bacterial populations. In Alphaproteobacteria, genes homologous to the “head–tail” gene cluster that encodes structural components of the Rhodobacter capsulatus GTA (RcGTA) are found in many taxa, even if they are only distantly related to Rhodobacter capsulatus. Yet, in most genomes available in GenBank RcGTA-like genes have annotations of typical viral proteins, and therefore are not easily distinguished from their viral homologs without additional analyses. Here, we report a “support vector machine” classifier that quickly and accurately distinguishes RcGTA-like genes from their viral homologs by capturing the differences in the amino acid composition of the encoded proteins. Our open-source classifier is implemented in Python and can be used to scan homologs of the RcGTA genes in newly sequenced genomes. The classifier can also be trained to identify other types of GTAs, or even to detect other elements of viral ancestry. Using the classifier trained on a manually curated set of homologous viruses and GTAs, we detected RcGTA-like “head–tail” gene clusters in 57.5% of the 1,423 examined alphaproteobacterial genomes. We also demonstrated that more than half of the in silico prophage predictions are instead likely to be GTAs, suggesting that in many alphaproteobacterial genomes the RcGTA-like elements remain unrecognized.


2012 ◽  
Vol 78 (16) ◽  
pp. 5555-5564 ◽  
Author(s):  
Atsushi Yoshii ◽  
Hiromitsu Moriyama ◽  
Toshiyuki Fukuhara

ABSTRACTKasugamycin (KSM), a unique aminoglycoside antibiotic, has been used in agriculture for many years to control not only rice blast caused by the fungusMagnaporthe griseabut also rice bacterial grain and seedling rot or rice bacterial brown stripe caused byBurkholderia glumaeorAcidovorax avenaesubsp.avenae, respectively. Since both bacterial pathogens are seed-borne and cause serious injury to rice seedlings, the emergence of KSM-resistantB. glumaeandA. avenaeisolates highlights the urgent need to understand the mechanism of resistance to KSM. Here, we identified a novel gene,aac(2′)-IIa, encoding a KSM 2′-N-acetyltransferase from both KSM-resistant pathogens but not from KSM-sensitive bacteria. AAC(2′)-IIa inactivates KSM, although it reveals no cross-resistance to other aminoglycosides. Theaac(2′)-IIagene fromB. glumaestrain 5091 was identified within the IncP genomic island inserted into the bacterial chromosome, indicating the acquisition of this gene by horizontal gene transfer. Although excision activity of the IncP island and conjugational gene transfer was not detected under the conditions tested, circular intermediates containing theaac(2′)-IIagene were detected. These results indicate that theaac(2′)-IIagene had been integrated into the IncP island of a donor bacterial species. Molecular detection of theaac(2′)-IIagene could distinguish whether isolates are resistant or susceptible to KSM. This may contribute to the production of uninfected rice seeds and lead to the effective control of these pathogens by KSM.


2019 ◽  
Vol 202 (2) ◽  
Author(s):  
Purvikalyan Pallegar ◽  
Lourdes Peña-Castillo ◽  
Evan Langille ◽  
Mark Gomelsky ◽  
Andrew S. Lang

ABSTRACT Gene transfer agents (GTAs) are bacteriophage-like particles produced by several bacterial and archaeal lineages that contain small pieces of the producing cells’ genomes that can be transferred to other cells in a process similar to transduction. One well-studied GTA is RcGTA, produced by the alphaproteobacterium Rhodobacter capsulatus. RcGTA gene expression is regulated by several cellular regulatory systems, including the CckA-ChpT-CtrA phosphorelay. The transcription of multiple other regulator-encoding genes is affected by the response regulator CtrA, including genes encoding putative enzymes involved in the synthesis and hydrolysis of the second messenger bis-(3′-5′)-cyclic dimeric GMP (c-di-GMP). To investigate whether c-di-GMP signaling plays a role in RcGTA production, we disrupted the CtrA-affected genes potentially involved in this process. We found that disruption of four of these genes affected RcGTA gene expression and production. We performed site-directed mutagenesis of key catalytic residues in the GGDEF and EAL domains responsible for diguanylate cyclase (DGC) and c-di-GMP phosphodiesterase (PDE) activities and analyzed the functions of the wild-type and mutant proteins. We also measured RcGTA production in R. capsulatus strains where intracellular levels of c-di-GMP were altered by the expression of either a heterologous DGC or a heterologous PDE. This adds c-di-GMP signaling to the collection of cellular regulatory systems controlling gene transfer in this bacterium. Furthermore, the heterologous gene expression and the four gene disruptions had similar effects on R. capsulatus flagellar motility as found for gene transfer, and we conclude that c-di-GMP inhibits both RcGTA production and flagellar motility in R. capsulatus. IMPORTANCE Gene transfer agents (GTAs) are virus-like particles that move cellular DNA between cells. In the alphaproteobacterium Rhodobacter capsulatus, GTA production is affected by the activities of multiple cellular regulatory systems, to which we have now added signaling via the second messenger dinucleotide molecule bis-(3′-5′)-cyclic dimeric GMP (c-di-GMP). Similar to the CtrA phosphorelay, c-di-GMP also affects R. capsulatus flagellar motility in addition to GTA production, with lower levels of intracellular c-di-GMP favoring increased flagellar motility and gene transfer. These findings further illustrate the interconnection of GTA production with global systems of regulation in R. capsulatus, providing additional support for the notion that the production of GTAs has been maintained in this and related bacteria because it provides a benefit to the producing organisms.


2021 ◽  
Vol 9 (6) ◽  
pp. 1115
Author(s):  
Kathryn Forcone ◽  
Felipe H. Coutinho ◽  
Giselle S. Cavalcanti ◽  
Cynthia B. Silveira

Roseobacters are globally abundant bacteria with critical roles in carbon and sulfur biogeochemical cycling. Here, we identified 173 new putative prophages in 79 genomes of Rhodobacteraceae. These prophages represented 1.3 ± 0.15% of the bacterial genomes and had no to low homology with reference and metagenome-assembled viral genomes from aquatic and terrestrial ecosystems. Among the newly identified putative prophages, 35% encoded auxiliary metabolic genes (AMGs), mostly involved in secondary metabolism, amino acid metabolism, and cofactor and vitamin production. The analysis of integration sites and gene homology showed that 22 of the putative prophages were actually gene transfer agents (GTAs) similar to a GTA of Rhodobacter capsulatus. Twenty-three percent of the predicted prophages were observed in the TARA Oceans viromes generated from free viral particles, suggesting that they represent active prophages capable of induction. The distribution of these prophages was significantly associated with latitude and temperature. The prophages most abundant at high latitudes encoded acpP, an auxiliary metabolic gene involved in lipid synthesis and membrane fluidity at low temperatures. Our results show that prophages and gene transfer agents are significant sources of genomic diversity in roseobacter, with potential roles in the ecology of this globally distributed bacterial group.


2018 ◽  
Vol 56 (1) ◽  
pp. 161-180 ◽  
Author(s):  
George W. Sundin ◽  
Nian Wang

Antibiotics have been used for the management of relatively few bacterial plant diseases and are largely restricted to high-value fruit crops because of the expense involved. Antibiotic resistance in plant-pathogenic bacteria has become a problem in pathosystems where these antibiotics have been used for many years. Where the genetic basis for resistance has been examined, antibiotic resistance in plant pathogens has most often evolved through the acquisition of a resistance determinant via horizontal gene transfer. For example, the strAB streptomycin-resistance genes occur in Erwinia amylovora, Pseudomonas syringae, and Xanthomonas campestris, and these genes have presumably been acquired from nonpathogenic epiphytic bacteria colocated on plant hosts under antibiotic selection. We currently lack knowledge of the effect of the microbiome of commensal organisms on the potential of plant pathogens to evolve antibiotic resistance. Such knowledge is critical to the development of robust resistance management strategies to ensure the safe and effective continued use of antibiotics in the management of critically important diseases.


2017 ◽  
Author(s):  
Migun Shakya ◽  
Shannon M. Soucy ◽  
Olga Zhaxybayeva

AbstractSeveral bacterial and archaeal lineages produce nanostructures that morphologically resemble small tailed viruses, but, unlike most viruses, contain apparently random pieces of the host genome. Since these elements can deliver the packaged DNA to other cells, they were dubbed Gene Transfer Agents (GTAs). Because many genes involved in GTA production have viral homologs, it has been hypothesized that the GTA ancestor was a virus. Whether GTAs represent an atypical virus, a defective virus, or a virus co-opted by the prokaryotes for some function, remains to be elucidated. To evaluate these possibilities, we examined the distribution and evolutionary histories of genes that encode a GTA in the α-proteobacteriumRhodobacter capsulatus(RcGTA). We report that although homologs of many individual RcGTA genes are abundant across bacteria and their viruses, RcGTA-like genomes are mainly found in one subclade of α-proteobacteria. When compared to the viral homologs, genes of the RcGTA-like genomes evolve significantly slower, and do not have higher %A+T nucleotides than their host chromosomes. Moreover, they appear to reside in stable regions of the bacterial chromosomes that are generally conserved across taxonomic orders. These findings argue against RcGTA being an atypical or a defective virus. Our phylogenetic analyses suggest that RcGTA ancestor likely originated in the lineage that gave rise to contemporary α-proteobacterial ordersRhizobiales, Rhodobacterales, Caulobacterales, Parvularculales, and Sphingomonadales,and since that time the RcGTA-like element has co-evolved with its host chromosomes. Such evolutionary history is compatible with maintenance of these elements by bacteria due to some selective advantage. As for many other prokaryotic traits, horizontal gene transfer played a substantial role in the evolution of RcGTA-like elements, not only in shaping its genome components within the orders, but also in occasional dissemination of RcGTA-like regions across the orders and even to different bacterial phyla.


2017 ◽  
Vol 64 (1) ◽  
Author(s):  
Wojciech Sledz ◽  
Sabina Zoledowska ◽  
Agata Motyka ◽  
Leszek Kadzinski ◽  
Bogdan Banecki

Animal manures are routinely applied to agricultural lands to improve crop yield, but the possibility to spread bacterial phytopathogens during field fertilizing has not been considered yet. We monitored 49 cattle, horse, swine, sheep or chicken manure samples collected in 14 Polish voivodeships for the most important plant pathogenic bacteria - Ralstonia solanacearum (Rsol), Xanthomonas campestris pv. campestris (Xcc), Pectobacterium carotovorum subsp. carotovorum (Pcc), Pectobacterium atrosepticum (Pba), Erwinia amylovora, Clavibacter michiganensis subsp. sepedonicus and Dickeya sp. All tested animal fertilizers were free of these pathogens. Subsequently, the growth dynamics of Pba, Pcc, Rsol, and Xcc in cattle, horse, swine, sheep and chicken manures sterilized either by autoclaving or filtration was evaluated. Investigated phytopathogens did not exhibit any growth in the poultry manure. However, the manure filtrates originating from other animals were suitable for microbial growth, resulting in the optical density change ranging 0.03 - 0.22, depending on bacterial species and the manure source. Pcc and Pba multiplied most efficiently in the cattle manure filtrate. These bacteria grew faster than Rsol and Xcc in all tested manure samples, both filtrates and the autoclaved semi-solid ones. Though, the growth dynamics of investigated strains in different animal fertilizers was unequal, all tested bacterial plant pathogens were proven to use cattle, horse, swine and sheep manures as the sources of nutrients. These findings may contribute to further research on the alternative routes of spread of bacterial phytopathogens, especially because of the fact that the control of pectionolytic bacteria is based only on prevention methods.


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