Analysis of transduction in wastewater bacterial populations by targeting the phage-derived 16S rRNA gene sequences

Casale, Antonio Del; Flanagan, Paul; Larkin, Michael J.; Allen, Christopher C. R.; Kulakov, Leonid

doi:10.1111/j.1574-6941.2010.01034.x

Cited by 29 publications

(18 citation statements)

References 34 publications

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“…Transduction has been documented in natural settings, including freshwater 107 , marine 108 , plant-associated 109 , rumen 110 , milk 106 and wastewater 111,112 environments. The wastewater studies are particularly revealing about the ability of phages to carry host genes, as these studies identify diverse bacterial 16S ribosomal DNA sequences in the viral component of the waste water 111,112 .…”

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“…The wastewater studies are particularly revealing about the ability of phages to carry host genes, as these studies identify diverse bacterial 16S ribosomal DNA sequences in the viral component of the waste water 111,112 . Some phages are thought to carry cellular genes because of a selective advantage that is accrued by the phage host, as exemplified by the photosynthesis genes that are carried by cyanophages 113 .…”

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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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Gene transfer agents: phage-like elements of genetic exchange

2012

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“…2). It has previously been shown that environmental phages in wastewater, sludge and soil contain 16S rRNA genes of bacterial origin (Sander & Schmieger, 2001, Del Casale et al, 2011aParsley et al, 2010;Ghosh et al, 2008).…”

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Evidence of bacteriophage-mediated horizontal transfer of bacterial 16S rRNA genes in the viral metagenome of the marine sponge Hymeniacidon perlevis

et al. 2012

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Evidence of bacteriophage-mediated horizontal transfer of bacterial 16S rRNA genes in the viral metagenome of the marine sponge Hymeniacidon perlevis Catriona Harrington, 1,2,3 Antonio Del Casale, 3 Jonathan Kennedy, 1 Horst Neve, 4 Bernard E. Picton, 5 Marlies J. Mooij, 1,2,6 Fergal O'Gara, 1,2,6 Leonid A. Kulakov, 3 Marine sponges have never been directly examined with respect to the presence of viruses or their potential involvement in horizontal gene transfer. Here we demonstrate for the first time, to our knowledge, the presence of viruses in the marine sponge Hymeniacidon perlevis. Moreover, bacterial 16S rDNA was detected in DNA isolated from these viruses, indicating that phagederived transduction appears to occur in H. perlevis. Phylogenetic analysis revealed that bacterial 16S rDNA isolated from sponge-derived viral and total DNA differed significantly, indicating that not all species are equally involved in transduction. INTRODUCTIONViruses are the most numerous and diverse biological entities in not only the marine environment, with 10 6 to 10 9 particles (ml seawater) 21 (Kristensen et al., 2010) and 10 30 unique viral genotypes (Suttle, 2007), but also on Earth (Angly et al., 2006). Viruses are extremely important life forms known to play a crucial role in microbial ecosystems. They are essential for maintaining and influencing the diversity of all microbial communities both by affecting them directly (by controlling numbers of bacterial cells) and by horizontally transferring genetic material to the host via the transduction process (Lohr et al., 2005). Phages can also affect microbial evolution as killing certain dominant bacteria may allow other related strains that are resistant to the phage to become dominant (Angly et al., 2006) in what is known as the 'kill the winner' hypothesis. This may help explain microbial diversity and the changes that can be observed within bacterial community composition ). However, this interaction between phages and their bacterial hosts has remained largely under studied, especially with respect to marine sponge ecosystems.Microbial communities of marine sponges are a major focus of current research, as sponge-associated microbes have been shown to produce a plethora of novel bioactive metabolites (Taylor et al., 2007). Due to the advent of high throughput sequencing, numerous metagenomic studies have facilitated the identification of sponge-associated bacterial groups, which have revealed remarkable levels of bacterial diversity, with 26 major phyla to date having been found to be present in close association with sponge species worldwide (Kennedy et al., 2008;Webster & Taylor 2012;Jackson et al., 2012). Some sponges have a low microbial abundance, with a microbial range similar to that of Abbreviations: CRISPR, clustered regularly interspaced short palindromic repeat; OTU, operational taxonomic unit; TEM, transmission electron microscopy; TFF, tangential flow filtration.The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequences from viral DN...

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“…Several studies point out that the bacterial rRNA gene can be packed into generalized transducing phage particles (2,5,13). We recently showed that an analysis of 16S rRNA gene sequences in the phage metagenome can be successfully used to study bacteria included in horizontal gene transfer mediated by transduction (4). In the current study, we analyzed 16S rRNA genes present in bacteriophage-derived (PH) and total (TOT) bacterial metagenomes isolated from wastewater over a 1-year period in order to assess the likely extent of transductional transfer in this environment.…”

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“…Samples Proteobacteria Alphaproteobacteria preparation was achieved as described previously (1,4). All DNA manipulations were performed using standard techniques (12).…”

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