Rhodobacter capsulatus genes encoding form I ribulose-1,5-bisphosphate carboxylase/oxygenase (cbbLS) and neighbouring genes were acquired by a horizontal gene transfer

ABSTRACTSeveral members of theRhodobacterales(Alphaproteobacteria) produce a conserved horizontal gene transfer vector, called the gene transfer agent (GTA), that appears to have evolved from a bacteriophage. The model system used to study GTA biology is theRhodobacter capsulatusGTA (RcGTA), a small, tailed bacteriophage-like particle produced by a subset of the cells in a culture. The response regulator CtrA is conserved in theAlphaproteobacteriaand is an essential regulator of RcGTA production: it controls the production and maturation of the RcGTA particle and RcGTA release from cells. CtrA also controls the natural transformation-like system required for cells to receive RcGTA-donated DNA. Here, we report that dysregulation of the CckA-ChpT-CtrA phosphorelay either by the loss of the PAS domain protein DivL or by substitution of the autophosphorylation residue of the hybrid histidine kinase CckA decreased CtrA phosphorylation and greatly increased RcGTA protein production inR. capsulatus. We show that the loss of the ClpXP protease or the three C-terminal residues of CtrA results in increased CtrA levels inR. capsulatusand identify ClpX(P) to be essential for the maturation of RcGTA particles. Furthermore, we show that CtrA phosphorylation is important for head spike production. Our results provide novel insight into the regulation of CtrA and GTAs in theRhodobacterales.IMPORTANCEMembers of theRhodobacteralesare abundant in ocean and freshwater environments. The conserved GTA produced by manyRhodobacteralesmay have an important role in horizontal gene transfer (HGT) in aquatic environments and provide a significant contribution to their adaptation. GTA production is controlled by bacterial regulatory systems, including the conserved CckA-ChpT-CtrA phosphorelay; however, several questions about GTA regulation remain. Our identification that a short DivL homologue and ClpXP regulate CtrA inR. capsulatusextends the model of CtrA regulation fromCaulobacter crescentusto a member of theRhodobacterales. We found that the magnitude of RcGTA production greatly depends on DivL and CckA kinase activity, adding yet another layer of regulatory complexity to RcGTA. RcGTA is known to undergo CckA-dependent maturation, and we extend the understanding of this process by showing that the ClpX chaperone is required for formation of tailed, DNA-containing particles.

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Homologues of Genetic Transformation DNA Import Genes Are Required for Rhodobacter capsulatus Gene Transfer Agent Recipient Capability Regulated by the Response Regulator CtrA

Journal of Bacteriology ◽

10.1128/jb.00332-15 ◽

2015 ◽

Vol 197 (16) ◽

pp. 2653-2663 ◽

Cited By ~ 29

Author(s):

Cedric A. Brimacombe ◽

Hao Ding ◽

Jeanette A. Johnson ◽

J. Thomas Beatty

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Rhodobacter Capsulatus ◽

Natural Transformation ◽

Response Regulator ◽

Content Type ◽

Gene Acquisition ◽

Metabolic Properties ◽

Cell Genome ◽

Key Aspects

ABSTRACTGene transfer agents (GTAs) morphologically resemble small, double-stranded DNA (dsDNA) bacteriophages; however, their only known role is to package and transfer random pieces of the producing cell genome to recipient cells. The best understood GTA is that ofRhodobacter capsulatus, termed RcGTA. We discovered that homologues of three genes involved in natural transformation in other bacteria,comEC,comF, andcomM, are essential for RcGTA-mediated gene acquisition. This paper gives genetic and biochemical evidence that RcGTA-borne DNA entry into cells requires the ComEC and ComF putative DNA transport proteins and genetic evidence that putative cytoplasmic ComM protein of unknown function is required for recipient capability. Furthermore, the master regulator of RcGTA production in <1% of a cell population, CtrA, which is also required for gene acquisition in recipient cells, is expressed in the vast majority of the population. Our results indicate that RcGTA-mediated gene transfer combines key aspects of two bacterial horizontal gene transfer mechanisms, where donor DNA is packaged in transducing phage-like particles and recipient cells take up DNA using natural transformation-related machinery. Both of these differentiated subsets of a culture population, donors and recipients, are dependent on the same response regulator, CtrA.IMPORTANCEHorizontal gene transfer (HGT) is a major driver of bacterial evolution and adaptation to environmental stresses. Traits such as antibiotic resistance or metabolic properties can be transferred between bacteria via HGT; thus, HGT can have a tremendous effect on the fitness of a bacterial population. The three classically described HGT mechanisms are conjugation, transformation, and phage-mediated transduction. More recently, the HGT factor GTA was described, where random pieces of producing cell genome are packaged into phage-like particles that deliver DNA to recipient cells. In this report, we show that transport of DNA borne by theR. capsulatusRcGTA into recipient cells requires key genes previously thought to be specific to natural transformation pathways. These findings indicate that RcGTA combines central aspects of phage-mediated transduction and natural transformation in an efficient, regulated mode of HGT.

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Novel 4-Chlorophenol Degradation Gene Cluster and Degradation Route via Hydroxyquinol in Arthrobacter chlorophenolicus A6

Applied and Environmental Microbiology ◽

10.1128/aem.71.11.6538-6544.2005 ◽

2005 ◽

Vol 71 (11) ◽

pp. 6538-6544 ◽

Cited By ~ 81

Author(s):

Karolina Nordin ◽

Maria Unell ◽

Janet K. Jansson

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Gene Cluster ◽

Microbial Degradation ◽

Codon Bias ◽

Sequence Similarity ◽

Open Reading Frames ◽

Genes Encoding ◽

Arthrobacter Chlorophenolicus ◽

Reading Frames

ABSTRACT Arthrobacter chlorophenolicus A6, a previously described 4-chlorophenol-degrading strain, was found to degrade 4-chlorophenol via hydroxyquinol, which is a novel route for aerobic microbial degradation of this compound. In addition, 10 open reading frames exhibiting sequence similarity to genes encoding enzymes involved in chlorophenol degradation were cloned and designated part of a chlorophenol degradation gene cluster (cph genes). Several of the open reading frames appeared to encode enzymes with similar functions; these open reading frames included two genes, cphA-I and cphA-II, which were shown to encode functional hydroxyquinol 1,2-dioxygenases. Disruption of the cphA-I gene yielded a mutant that exhibited negligible growth on 4-chlorophenol, thereby linking the cph gene cluster to functional catabolism of 4-chlorophenol in A. chlorophenolicus A6. The presence of a resolvase pseudogene in the cph gene cluster together with analyses of the G+C content and codon bias of flanking genes suggested that horizontal gene transfer was involved in assembly of the gene cluster during evolution of the ability of the strain to grow on 4-chlorophenol.

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Physiological Control and Regulation of the Rhodobacter capsulatus cbb Operons

Journal of Bacteriology ◽

10.1128/jb.180.16.4258-4269.1998 ◽

1998 ◽

Vol 180 (16) ◽

pp. 4258-4269 ◽

Cited By ~ 47

Author(s):

George C. Paoli ◽

Padungsri Vichivanives ◽

F. Robert Tabita

Keyword(s):

Rhodobacter Capsulatus ◽

Pentose Phosphate ◽

Open Reading Frames ◽

Physiological Control ◽

Gene Encoding ◽

Bisphosphate Carboxylase ◽

Promoter Fusion ◽

Fructose 1,6 Bisphosphatase ◽

Mutant Strains ◽

Genes Encoding

ABSTRACT The genes encoding enzymes of the Calvin-Benson-Bassham (CBB) reductive pentose phosphate pathway in Rhodobacter capsulatus are organized in at least two operons, each preceded by a separate cbbR gene, encoding potential LysR-type transcriptional activators. As a prelude to studies ofcbb gene regulation in R. capsulatus, the nucleotide sequence of a 4,537-bp region, which includedcbbR II, was determined. This region contained the following open reading frames: a partial pgmgene (encoding phosphoglucomutase) and a complete qorgene (encoding NADPH:quinone oxidoreductase), followed by cbbR II, cbbF (encoding fructose 1,6-bisphosphatase), cbbP (encoding phosphoribulokinase), and part of cbbT (encoding transketolase). Physiological control of the CBB pathway and regulation of the R. capsulatus cbb genes were studied by using a combination of mutant strains and promoter fusion constructs. Characterization of mutant strains revealed that either form I or form II ribulose 1,5-bisphosphate carboxylase/oxygenase (RubisCO), encoded by the cbbLS andcbbM genes, respectively, could support photoheterotrophic and autotrophic growth. A strain with disruptions in both cbbL and cbbM could not grow autotrophically and grew photoheterotrophically only when dimethyl sulfoxide was added to the culture medium. Disruption ofcbbP resulted in a strain that did not synthesize form II RubisCO and had a phenotype similar to that observed in the RubisCO-minus strain, suggesting that there is only onecbbP gene in R. capsulatus and that this gene is cotranscribed with cbbM. Analysis of RubisCO activity and synthesis in strains with disruptions in eithercbbR I orcbbR II, and β-galactosidase determinations from wild-type and mutant strains containing cbb Ip- andcbb IIp-lacZ fusion constructs, indicated that the cbb I andcbb II operons of R. capsulatus are within separate CbbR regulons.

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Horizontal Transfer of Bacterial Cytolethal Distending Toxin B Genes to Insects

Molecular Biology and Evolution ◽

10.1093/molbev/msz146 ◽

2019 ◽

Vol 36 (10) ◽

pp. 2105-2110 ◽

Cited By ~ 2

Author(s):

Kirsten I Verster ◽

Jennifer H Wisecaver ◽

Marianthi Karageorgi ◽

Rebecca P Duncan ◽

Andrew D Gloss ◽

...

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Natural Enemies ◽

Larval Stage ◽

Horizontal Transfer ◽

Parasitoid Wasps ◽

Cytolethal Distending Toxin ◽

Toxin B ◽

Genes Encoding ◽

Hamiltonella Defensa

Abstract Horizontal gene transfer events have played a major role in the evolution of microbial species, but their importance in animals is less clear. Here, we report horizontal gene transfer of cytolethal distending toxin B (cdtB), prokaryotic genes encoding eukaryote-targeting DNase I toxins, into the genomes of vinegar flies (Diptera: Drosophilidae) and aphids (Hemiptera: Aphididae). We found insect-encoded cdtB genes are most closely related to orthologs from bacteriophage that infect Candidatus Hamiltonella defensa, a bacterial mutualistic symbiont of aphids that confers resistance to parasitoid wasps. In drosophilids, cdtB orthologs are highly expressed during the parasitoid-prone larval stage and encode a protein with ancestral DNase activity. We show that cdtB has been domesticated by diverse insects and hypothesize that it functions in defense against their natural enemies.

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The genome of the mustard leaf beetle encodes two active xylanases originally acquired from bacteria through horizontal gene transfer

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2013.1021 ◽

2013 ◽

Vol 280 (1763) ◽

pp. 20131021 ◽

Cited By ~ 52

Author(s):

Yannick Pauchet ◽

David G. Heckel

Keyword(s):

Cell Wall ◽

Gene Transfer ◽

Horizontal Gene Transfer ◽

Plant Cell ◽

Plant Cell Wall ◽

Genetic Material ◽

Leaf Beetle ◽

Glycoside Hydrolase Family ◽

Cell Wall Degrading Enzymes ◽

Genes Encoding

The primary plant cell wall comprises the most abundant polysaccharides on the Earth and represents a rich source of energy for organisms which have evolved the ability to digest them. Enzymes able to degrade plant cell wall polysaccharides are widely distributed in micro-organisms but are generally absent in animals, although their presence in insects, especially phytophagous beetles from the superfamilies Chrysomeloidea and Curculionoidea, has recently begun to be appreciated. The observed patchy distribution of endogenous genes encoding these enzymes in animals has raised questions about their evolutionary origins. Recent evidence suggests that endogenous plant cell wall degrading enzymes-encoding genes have been acquired by animals through a mechanism known as horizontal gene transfer (HGT). HGT describes how genetic material is moved by means other than vertical inheritance from a parent to an offspring. Here, we provide evidence that the mustard leaf beetle, Phaedon cochleariae , possesses in its genome genes encoding active xylanases from the glycoside hydrolase family 11 (GH11). We also provide evidence that these genes were originally acquired by P. cochleariae from a species of gammaproteobacteria through HGT. This represents the first example of the presence of genes from the GH11 family in animals.

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Metabolic Signals That Lead to Control of CBB Gene Expression in Rhodobacter capsulatus

Journal of Bacteriology ◽

10.1128/jb.184.7.1905-1915.2002 ◽

2002 ◽

Vol 184 (7) ◽

pp. 1905-1915 ◽

Cited By ~ 25

Author(s):

Mary A. Tichi ◽

F. Robert Tabita

Keyword(s):

Gene Expression ◽

Rhodobacter Capsulatus ◽

Pentose Phosphate ◽

Gene Encoding ◽

Bisphosphate Carboxylase ◽

Starting Point ◽

Mutant Strains ◽

Genes Encoding ◽

Metabolic Signal ◽

Made In

ABSTRACT Various mutant strains were used to examine the regulation and metabolic control of the Calvin-Benson-Bassham (CBB) reductive pentose phosphate pathway in Rhodobacter capsulatus. Previously, a ribulose 1,5-bisphosphate carboxylase/oxygenase (RubisCO)-deficient strain (strain SBI/II) was found to show enhanced levels of cbb I and cbb II promoter activities during photoheterotrophic growth in the presence of dimethyl sulfoxide. With this strain as the starting point, additional mutations were made in genes encoding phosphoribulokinase and transketolase and in the gene encoding the LysR-type transcriptional activator, CbbRII. These strains revealed that a product generated by phosphoribulokinase was involved in control of CbbR-mediated cbb gene expression in SBI/II. Additionally, heterologous expression experiments indicated that Rhodobacter sphaeroides CbbR responded to the same metabolic signal in R. capsulatus SBI/II and mutant strain backgrounds.

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Horizontally transferred genes in the ctenophore Mnemiopsis leidyi

10.7287/peerj.preprints.3462 ◽

2018 ◽

Author(s):

Alexandra M Hernandez ◽

Joseph F Ryan

Keyword(s):

Antibiotic Resistance ◽

Gene Transfer ◽

Horizontal Gene Transfer ◽

Genetic Information ◽

Mnemiopsis Leidyi ◽

Uncharacterized Protein ◽

Phylogenetic Incongruence ◽

Wide Range ◽

Growing Body ◽

Genes Encoding

Horizontal gene transfer has had major impacts on the biology of a wide range of organisms from antibiotic resistance in bacteria to adaptations to herbivory in arthropods. A growing body of literature shows that horizontal gene transfer (HGT) between non-animals and animals is more commonplace than previously thought. In this study, we present a thorough investigation of HGT in the ctenophore Mnemiopsis leidyi. We applied tests of phylogenetic incongruence to identify nine genes that were likely transferred horizontally early in ctenophore evolution from bacteria and non-metazoan eukaryotes. All but one of these HGTs (an uncharacterized protein) are homologous to characterized enzymes, supporting previous observations that genes encoding enzymes are more likely to be retained after HGT events. We found that the majority of these nine horizontally transferred genes were expressed during development, suggesting that they are active and play a role in the biology of M. leidyi. This is the first report of HGT in ctenophores, and contributes to an ever-growing literature on the prevalence of genetic information flowing between non-animals and animals.

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Horizontally transferred genes in the ctenophore Mnemiopsis leidyi

10.7287/peerj.preprints.3462v3 ◽

2018 ◽

Author(s):

Alexandra M Hernandez ◽

Joseph F Ryan

Keyword(s):

Antibiotic Resistance ◽

Gene Transfer ◽

Horizontal Gene Transfer ◽

Genetic Information ◽

Mnemiopsis Leidyi ◽

Uncharacterized Protein ◽

Phylogenetic Incongruence ◽

Wide Range ◽

Growing Body ◽

Genes Encoding

Horizontal gene transfer has had major impacts on the biology of a wide range of organisms from antibiotic resistance in bacteria to adaptations to herbivory in arthropods. A growing body of literature shows that horizontal gene transfer (HGT) between non-animals and animals is more commonplace than previously thought. In this study, we present a thorough investigation of HGT in the ctenophore Mnemiopsis leidyi. We applied tests of phylogenetic incongruence to identify nine genes that were likely transferred horizontally early in ctenophore evolution from bacteria and non-metazoan eukaryotes. All but one of these HGTs (an uncharacterized protein) are homologous to characterized enzymes, supporting previous observations that genes encoding enzymes are more likely to be retained after HGT events. We found that the majority of these nine horizontally transferred genes were expressed during development, suggesting that they are active and play a role in the biology of M. leidyi. This is the first report of HGT in ctenophores, and contributes to an ever-growing literature on the prevalence of genetic information flowing between non-animals and animals.

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