Evolutionary Implications of Phylogenetic Analyses of the Gene Transfer Agent (GTA) of Rhodobacter capsulatus

Lang, Andrew S.; Taylor, Terumi A.; Beatty, J. Thomas

doi:10.1007/s00239-002-2348-7

Cited by 40 publications

(31 citation statements)

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“…Apparently, GTA evolved in the chromosome under the control of the cell cycle and growth phase (57). Similar genetic elements are widespread in bacteria and possibly archaea.…”

Section: Involvement Of Holins In Bacterial Gene Transfermentioning

confidence: 98%

Holins in Bacteria, Eukaryotes, and Archaea: Multifunctional Xenologues with Potential Biotechnological and Biomedical Applications

2015

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bHolins form pores in the cytoplasmic membranes of bacteria for the primary purpose of releasing endolysins that hydrolyze the cell wall and induce cell death. Holins are encoded within bacteriophage genomes, where they promote cell lysis for virion release, and within bacterial genomes, where they serve a diversity of potential or established functions. These include (i) release of gene transfer agents, (ii) facilitation of programs of differentiation such as those that allow sporulation and spore germination, (iii) contribution to biofilm formation, (iv) promotion of responses to stress conditions, and (v) release of toxins and other proteins. There are currently 58 recognized families of holins and putative holins with members exhibiting between 1 and 4 transmembrane ␣-helical spanners, but many more families have yet to be discovered. Programmed cell death in animals involves holin-like proteins such as Bax and Bak that may have evolved from bacterial holins. Holin homologues have also been identified in archaea, suggesting that these proteins are ubiquitous throughout the three domains of life. Phage-mediated cell lysis of dualmembrane Gram-negative bacteria also depends on outer membrane-disrupting "spanins" that function independently of, but in conjunction with, holins and endolysins. In this minireview, we provide an overview of their modes of action and the first comprehensive summary of the many currently recognized and postulated functions and uses of these cell lysis systems. It is anticipated that future studies will result in the elucidation of many more such functions and the development of additional applications.

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“…Apparently, GTA evolved in the chromosome under the control of the cell cycle and growth phase (57). Similar genetic elements are widespread in bacteria and possibly archaea.…”

Section: Involvement Of Holins In Bacterial Gene Transfermentioning

confidence: 98%

Holins in Bacteria, Eukaryotes, and Archaea: Multifunctional Xenologues with Potential Biotechnological and Biomedical Applications

2015

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“…An RcGTA-like gene cluster was first identified in another purple photosynthetic bacterium, Rhodopseudomonas palustris 37 , followed by clusters in Rhodobacter sphaeroides, Caulobacter crescentus, Agrobacterium tumefaciens and Brucella melitensis 42 , and then other species as additional complete genome sequences became available 28,43,44 . To date, RcGTA-like genes have been found in all taxonomic orders that are represented by complete genome sequences in the class Alphaproteobacteria (FIG.…”

Section: Gtas In Other Alphaproteobacteriamentioning

confidence: 99%

Gene transfer agents: phage-like elements of genetic exchange

2012

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Horizontal gene transfer is important in the evolution of bacterial and archaeal genomes. An interesting genetic exchange process is carried out by diverse phage-like gene transfer agents (GTAs) that are found in a wide range of prokaryotes. Although GTAs resemble phages, they lack the hallmark capabilities that define typical phages, and they package random pieces of the producing cell's genome. In this Review, we discuss the defining characteristics of the GTAs that have been identified to date, along with potential functions for these agents and the possible evolutionary forces that act on the genes involved in their production.The prevalence of horizontal gene transfer (HGT), in which DNA is exchanged between closely or distantly related lineages, has altered the way we think about evolution 1,2 , having profound effects on our views of the evolutionary relationships among living organisms. It has caused a shift from a bifurcating 'tree of life' view to a 'net of life' or 'web of life' view [3][4][5] , in which "highways of gene sharing" (REF. 6) represent major connections, with genes (or DNA segments) viewed as "public goods, available for all organisms to integrate into their genomes" (REF. 7). HGT occurs within and between all three domains of life, and it has been estimated that 0.05-80% of genes in bacterial and archaeal genomes have been affected by HGT, depending on the analytical method used and the genome analysed [8][9][10] . Although HGT is widespread, it is not random: patterns of preferential gene exchange among specific groups of organisms that share ancestry or habitat have been * Present address. aslang@mun.ca; olgazh@dartmouth.edu; j.beatty@mail.ubc.ca Competing interests statementThe authors declare no competing financial interests. 6,9,11,12 . Such patterns are probably a consequence of existing barriers to HGT, which have been reviewed in detail elsewhere 13,14 . FURTHER INFORMATIONAlthough we have known about some HGT mechanisms for decades, novel processes that expand the existing repertoire of gene exchange methods are continually being identified. Transformation was the first mechanism of gene exchange to be discovered 15 , wherein DNA is taken up directly from the environment (reviewed elsewhere 16,17 ). In transduction, DNA transfer is mediated by viral particles (BOX 1). In conjugation, which was discovered in the 1940s 18 , DNA is transferred from a donor to a recipient cell during cell-to-cell contact; conjugation is used in the transfer of plasmids, transposons, integrons, and integrative and conjugative elements (ICEs) [19][20][21] . There are other modes of gene exchange that do not fit well into any of these three canonical mechanisms, including temporary cell fusion followed by chromosomal recombination and plasmid exchange 22 , intercellular connection through nanotubes 23 , and the release of membrane vesicles containing chromosomal, plasmid and phage DNA that can then merge with nearby cells 24 . In addition, a novel mechanism of gene transfer that has feature...

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“…There are 42 putative intact or mutated transposase genes and 237 phage-related genes. An important and specific feature of R. capsulatus is the defective phage called gene transfer agent (GTA) that provides a useful tool for genetic analysis (9). The distribution of genes among the COG metabolic functional classes and detailed descriptions of the metabolic pathways can be found at http://rhodo.img.cas.cz.…”

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confidence: 99%

Complete Genome Sequence of the Photosynthetic Purple Nonsulfur Bacterium Rhodobacter capsulatus SB 1003

et al. 2010

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Rhodobacter capsulatus SB 1003 belongs to the group of purple nonsulfur bacteria. Its genome consists of a 3.7-Mb chromosome and a 133-kb plasmid. The genome encodes genes for photosynthesis, nitrogen fixation, utilization of xenobiotic organic substrates, and synthesis of polyhydroxyalkanoates. These features made it a favorite research tool for studying these processes. Here we report its complete genome sequence.The genome of Rhodobacter capsulatus SB 1003 consists of a single chromosome containing 3,738,958 bp and a circular plasmid of 132,962 bp. Both the chromosome and the plasmid have relatively high GC content (66.6%) that made DNA sequencing difficult. The project was started by constructing a library of overlapping cosmids covering the whole genome (4, 5). Sequencing was performed by using standard Sanger approaches, and the average sequencing depth was 7. The complete sequence was analyzed by using Critica (1) and Glimmer (3) for the protein-coding genes, tRNAscan (11) and Aragorn (10) for the tRNA and tmRNA genes, and RNAmmer (8) for the rRNA genes. The functions of the predicted protein-coding genes were annotated by comparison with the UniRef90 (14), NCBI-NR (2), COG (15), and KEGG (7) databases. The annotation results were verified using Artemis (13) with dicodon use plots (12).We found 3,531 open reading frames (ORFs) in the chromosome and 154 ORFs in the plasmid. There are 4 rRNA operons and 53 tRNA genes for all 20 amino acids and one tmRNA gene. The coding density of the R. capsulatus genome is 91%. Functions were assigned to 3,100 ORFs (84.1%). Six hundred ten ORFs (16.6%) represent genes with some similarity to hypothetical genes in databases. The remaining ORFs had no homologues in the databases (e-value Ͻ 1 ϫ 10 Ϫ10 ). There are 42 putative intact or mutated transposase genes and 237 phage-related genes. An important and specific feature of R. capsulatus is the defective phage called gene transfer agent (GTA) that provides a useful tool for genetic analysis (9). The distribution of genes among the COG metabolic functional classes and detailed descriptions of the metabolic pathways can be found at http://rhodo.img.cas.cz. Based on the GC skew analysis and the orientation of transcription, the origin of replication was localized around 160 kb.Five complete restriction-modification (RM) systems were identified in the genome. Three of them are type I (RcaSBIP, RcaSBIIIP, and RcaSBIV), one is type III (RcaSBIIP), and one is a type IV system (RcaSBMcrBCP). These RM systems are located mainly in regions of exogenic origin. Several genes encoding these restriction and modification enzymes were isolated and characterized. RcaSBIV recognizes the sequence AGAN7RTAG (H. Strnad and V. Paces, unpublished). Eight CRISPR/Cas systems (6), of which two comprise a considerable number of repetitions (41 and 9), were also found. The others comprise three to five repetitions.Nucleotide sequence accession numbers. The nucleotide sequences were deposited in GenBank with accession numbers CP001312 (chromosome) and...

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Evolutionary Implications of Phylogenetic Analyses of the Gene Transfer Agent (GTA) of Rhodobacter capsulatus

Cited by 40 publications

References 0 publications

Holins in Bacteria, Eukaryotes, and Archaea: Multifunctional Xenologues with Potential Biotechnological and Biomedical Applications

Holins in Bacteria, Eukaryotes, and Archaea: Multifunctional Xenologues with Potential Biotechnological and Biomedical Applications

Gene transfer agents: phage-like elements of genetic exchange

Complete Genome Sequence of the Photosynthetic Purple Nonsulfur Bacterium Rhodobacter capsulatus SB 1003

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