Phylogeographic reconstruction of a bacterial species with high levels of lateral gene transfer

Pearson, Talima; Giffard, Philip M.; Beckstrom-Sternberg, Stephen M.; Auerbach, Raymond K.; Hornstra, Heidie; Tuanyok, Apichai; Price, Erin P.; Glass, Mindy B.; Leadem, Benjamin R.; Beckstrom-Sternberg, James S.; Allan, Gerard J.; Foster, Jeffrey T.; Wagner, David M.; Okinaka, Richard T.; Sim, Siew Hoon; Pearson, Ofori N.; Wu, Zaining; Chang, Jean; Kaul, Rajinder; Hoffmaster, Alex R.; Brettin, Thomas; Robison, Richard A.; Mayo, Mark; Gee, Jay E.; Tan, Patrick; Currie, Bart J.; Keim, Paul

doi:10.1186/1741-7007-7-78

Cited by 163 publications

(227 citation statements)

References 80 publications

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“…Sampling strategies for bacterial population genomics As we discussed in the Introduction, genomes from a global collection of species can be valuable, for example, for assessing the pan-genome (Tettelin et al, 2005) or to design molecular markers (Pearson et al, 2009), whereas a metagenomic approach can provide information about diversity in a local context (Allen et al, 2007;Eppley et al, 2007). Both these strategies have limitations, however, and do not directly address the manner in which genetic …”

Section: Discussionmentioning

confidence: 99%

Population genomics of Sinorhizobium medicae based on low-coverage sequencing of sympatric isolates

et al. 2011

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We investigated the genomic diversity of a local population of the symbiotic bacterium Sinorhizobium medicae, isolated from the roots of wild Medicago lupulina plants, in order to assess genomic diversity, to identify genomic regions influenced by duplication, deletion or strong selection, and to explore the composition of the pan-genome. Partial genome sequences of 12 isolates were obtained by Roche 454 shotgun sequencing (average 5.3 Mb per isolate) and compared with the published sequence of S. medicae WSM 419. Homologous recombination appears to have less impact on the polymorphism patterns of the chromosome than on the chromid pSMED01 and megaplasmid pSMED02. Moreover, pSMED02 is a hot spot of insertions and deletions. The whole chromosome is characterized by low sequence polymorphism, consistent with the high density of housekeeping genes. Similarly, the level of polymorphism of symbiosis genes (low) and of genes involved in polysaccharide synthesis (high) may reflect different selection. Finally, some isolates carry genes that may confer adaptations that S. medicae WSM 419 lacks, including homologues of genes encoding rhizobitoxine synthesis, iron uptake, response to autoinducer-2, and synthesis of distinct polysaccharides. The presence or absence of these genes was confirmed by PCR in each of these 12 isolates and a further 27 isolates from the same population. All isolates had rhizobitoxine genes, while the other genes were co-distributed, suggesting that they may be on the same mobile element. These results are discussed in relation to the ecology of Medicago symbionts and in the perspective of population genomics studies.

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Section: Discussionmentioning

confidence: 99%

Population genomics of Sinorhizobium medicae based on low-coverage sequencing of sympatric isolates

et al. 2011

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“…Perhaps the most important question involves the relevance of our observations with Bt to pathogenesis in Bp and Bm. A recent analysis of the global population structure of Burkholderia species pathogenic for mammals predicts an Australian origin for Bp, with a single introduction event leading to the expansion of Southeast Asian isolates (SEA Bp) and Bm (29). Interestingly, the fla2 gene cluster is absent in SEA Bp isolates such as Bp340, which is dependent on BimA for plaque formation (Fig.…”

Section: Discussionmentioning

confidence: 99%

Dissection of the Burkholderia intracellular life cycle using a photothermal nanoblade

French

Toesca

Wu³

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

144

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Burkholderia pseudomallei and Burkholderia thailandensis are related pathogens that invade a variety of cell types, replicate in the cytoplasm, and spread to nearby cells. We have investigated temporal and spatial requirements for virulence determinants in the intracellular life cycle, using genetic dissection and photothermal nanoblade delivery, which allows efficient placement of bacterium-sized cargo into the cytoplasm of mammalian cells. The conserved Bsa type III secretion system (T3SS Bsa ) is dispensable for invasion, but is essential for escape from primary endosomes. By nanoblade delivery of B. thailandensis we demonstrate that all subsequent events in intercellular spread occur independently of T3SS Bsa activity. Although intracellular movement was essential for cell-cell spread by B. pseudomallei and B. thailandensis, neither BimA-mediated actin polymerization nor the formation of membrane protrusions containing bacteria was required for B. thailandensis. Surprisingly, the cryptic (fla2) flagellar system encoded on chromosome 2 of B. thailandensis supported rapid intracellular motility and efficient cell-cell spread. Plaque formation by both pathogens was dependent on the activity of a type VI secretion system (T6SS-1) that functions downstream from T3SS Bsa -mediated endosome escape. A remarkable feature of Burkholderia is their ability to induce the formation of multinucleate giant cells (MNGCs) in multiple cell types. By infection and nanoblade delivery, we observed complete correspondence between mutant phenotypes in assays for cell fusion and plaque formation, and time-course studies showed that plaque formation represents MNGC death. Our data suggest that the primary means for intercellular spread involves cell fusion, as opposed to pseudopod engulfment and bacterial escape from double-membrane vacuoles.

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“…However, the low substitution and indel mutation rates observed in this study need not imply limited genetic diversity among species of the B. cepacia complex. Rather, because of their high N e and evidently frequent lateral genetic transfer, species of the B. cepacia complex are remarkably diverse (Baldwin et al 2005;Pearson et al 2009), demonstrating that low mutation rates need not imply low levels of genetic diversity.…”

Section: Discussionmentioning

confidence: 99%

The Rate and Molecular Spectrum of Spontaneous Mutations in the GC-Rich Multichromosome Genome of Burkholderia cenocepacia

et al. 2015

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Spontaneous mutations are ultimately essential for evolutionary change and are also the root cause of many diseases. However, until recently, both biological and technical barriers have prevented detailed analyses of mutation profiles, constraining our understanding of the mutation process to a few model organisms and leaving major gaps in our understanding of the role of genome content and structure on mutation. Here, we present a genome-wide view of the molecular mutation spectrum in Burkholderia cenocepacia, a clinically relevant pathogen with high %GC content and multiple chromosomes. We find that B. cenocepacia has low genome-wide mutation rates with insertion-deletion mutations biased toward deletions, consistent with the idea that deletion pressure reduces prokaryotic genome sizes. Unlike prior studies of other organisms, mutations in B. cenocepacia are not AT biased, which suggests that at least some genomes with high %GC content experience unusual base-substitution mutation pressure. Importantly, we also observe variation in both the rates and spectra of mutations among chromosomes and elevated G:C . T:A transversions in late-replicating regions. Thus, although some patterns of mutation appear to be highly conserved across cellular life, others vary between species and even between chromosomes of the same species, potentially influencing the evolution of nucleotide composition and genome architecture.KEYWORDS mutation rate; genome evolution; replication timing; mutation spectra A S the ultimate source of genetic variation, mutation is implicit in every aspect of genetics and evolution. However, as a result of the genetic burden imposed by deleterious mutations, remarkably low mutation rates have evolved across all of life, making detection of these rare events technologically challenging and accurate measures of mutation rates and spectra exceedingly difficult (Kibota and Lynch 1996;Lynch and Walsh 1998;Sniegowski et al. 2000;Lynch 2011;Fijalkowska et al. 2012;Zhu et al. 2014). Until recently, most estimates of mutational properties have been derived indirectly using comparative genomics at putatively neutral sites (Graur and Li 2000;Wielgoss et al. 2011) or by extrapolation from small reporter-construct studies (Drake 1991). Both of these methods are subject to potentially significant biases, as many putatively neutral sites are subject to selection and mutation rates can vary substantially among different genomic regions (Lynch 2007).To avoid the potential biases of these earlier methods, pairing classic mutation accumulation (MA) with wholegenome sequencing (WGS) has become the preferred method for obtaining direct measures of mutation rates and spectra (Lynch et al. 2008;Denver et al. 2009;Ossowski et al. 2010;Lee et al. 2012; Sung et al. 2012a,b;Heilbron et al. 2014). Using this strategy, a single clonal ancestor is used to initiate several replicate lineages that are subsequently passaged through repeated single-cell bottlenecks for several thousand generations. The complete genomes of ea...

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Phylogeographic reconstruction of a bacterial species with high levels of lateral gene transfer

Cited by 163 publications

References 80 publications

Population genomics of Sinorhizobium medicae based on low-coverage sequencing of sympatric isolates

Population genomics of Sinorhizobium medicae based on low-coverage sequencing of sympatric isolates

Dissection of the Burkholderia intracellular life cycle using a photothermal nanoblade

The Rate and Molecular Spectrum of Spontaneous Mutations in the GC-Rich Multichromosome Genome of Burkholderia cenocepacia

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