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Genome Evolution in Burkholderia Spp

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Genome Evolution in Burkholderia Spp bioRxiv preprint doi: https://doi.org/10.1101/319723; this version posted May 10, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Genome evolution in Burkholderia spp Olga O Bochkareva1,2,*, Elena V Moroz1,**, Iakov I Davydov3,4,** and Mikhail S Gelfand1,2,5,6 1Kharkevich Institute for Information Transmission Problems, Moscow, Russia 2Center for Data-Intensive Biomedicine and Biotechnology, Skolkovo Institute of Science and Technology, Moscow, Russia 3Department of Ecology and Evolution & Department of Computational Biology, University of Lausanne, Lausanne, Switzerland 4Swiss Institute of Bioinformatics, Lausanne, Switzerland 5Faculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University, Moscow, Russia 6Faculty of Computer Science, Higher School of Economics, Moscow, Russia *corresponding author, [email protected] **equal contribution Abstract niches during species formation. Conclusions This study demonstrates the power of integrated analy- Background sis of pan-genomes, chromosome rearrangements, and The genus Burkholderia consists of species that oc- selection regimes. Non-random inversion patterns in- cupy remarkably diverse ecological niches. Its best dicate selective pressure, inversions are particularly known members are important pathogens, B. mallei frequent in a recent pathogen B. mallei, and, together and B. pseudomallei, which cause glanders and melioi- with periods of positive selection at other branches, dosis, respectively. Burkholderia genomes are unusual may indicate adaptation to new niches. One such adap- due to their multichromosomal organization. tation could be possible phase variation mechanism in Results B. pseudomallei. We performed pan-genome analysis of 127 Burkholde- Keywords ria strains. The pan-genome is open with the satura- multi-chromosome bacteria; genome rearrangements; tion to be reached between 86,000 and 88,000 genes. pan-genome; comparative genomics; strain phylogeny; The reconstructed rearrangements indicate a strong positive selection. avoidance of intra-replichore inversions that is likely caused by selection against the transfer of large groups of genes between the leading and the lagging strands. Background Translocated genes also tend to retain their position in the leading or the lagging strand, and this selection is The first evidence of multiple chromosomes stronger for large syntenies. in bacteria came from studies on Rhodobacter We detected parallel inversions in the second chro- sphaeroides (Suwanto and Kaplan, 1989). Known mosomes of seven B. pseudomallei. Breakpoints of these bacteria with multiple chromosome belong to the inversions are formed by genes encoding components Chloroflexi (Kiss et al., 2010), Cyanobacteria (Welsh of multidrug resistance complex. The membrane com- et al., 2008), Deinococcus-Thermus (White et al., ponents of this system are exposed to the host’s immune 1999), Firmicutes (Wegmann et al., 2014), Proteobacte- system, and hence these inversions may be linked to a ria (Holden et al., 2004), and Spirochaetes (Ren et al., phase variation mechanism. We identified 197 genes 2003) phyla. The organization of these genomes varies. evolving under positive selection. We found seventeen There could be linear and circular chromosomes as genes evolving under positive selection on individual in Agrobacterium tumefaciens (Allardet-Servent et al., branches; most of the positive selection periods map 1993) or several circular chromosomes as in Brucella to the branches that are ancestral to species clades. spp. (Michaux et al., 1993) or Burkholderia spp. (Lessie This might indicate rapid adaptation to new ecological et al., 1996). Species belonging to one genus may bioRxiv preprint doi: https://doi.org/10.1101/319723; this version posted May 10, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Genome evolution in Burkholderia spp have different numbers of chromosomes, for example Burkholderia genomes has been estimated to exceed Burkholderia cepacia has three chromosomes (Lessie 40,000 genes with no sign of saturation upon addition et al., 1996) while Burkholderia pseudomallei (Holden of more strains, and the core-genome is approximately et al., 2004), two. 1,000 genes (Ussery et al., 2009). A separate analysis In bacteria with multiple chromosomes, the majority of 37 complete B. pseudomallei genomes did not show of genes necessary for the basic life processes usually saturation either (Spring-Pearson et al., 2015). The are located on one (primary) chromosome. Other (sec- genomes of B. mallei demonstrate low genetic diversity ondary) chromosomes contain few essential genes and in comparison to B. pseudomallei (Ussery et al., 2009). are mainly composed of niche-specific genes (Egan, The core-genome of B. mallei is smaller than that of B. Fogel, and Waldor, 2005). An exception is two circular pseudomallei, while the variable gene sets are larger for chromosomes of Rhodobacter sphaeroides that share re- B. mallei (Losada et al., 2010). B. thailandensis, also sponsibilities for fundamental cell processes (Macken- belonging to the pseudomallei group, adds many genes zie et al., 2001). Usually genes on a secondary chro- to the pan-genome of B. mallei and B. pseudomallei mosome evolve faster than genes on a primary chro- but does not influence the core-genome (Ussery et al., mosome (Cooper et al., 2010). At that, secondary 2009). chromosomes may serve as evolutionary test beds so Several examples of gene translocations between that genes from secondary chromosomes provide con- chromosomes in Burkholderia are known, e.g., the ditional benefits in particular environments (Cooper translocation between the first and the third chromo- et al., 2010). Secondary chromosomes usually evolve somes in B. cenocepacia AU 1054, affecting many es- from plasmids (Egan, Fogel, and Waldor, 2005). The sential genes (Guo et al., 2010). Following interchro- plasmids may carry genes encoding traits beneficial for mosomal translocation, genes change their expression the organism’s survival, for example, resistance to an- level and substitution rate, dependent on the direction tibiotics or to heavy metals. Usually the plasmid size is of the translocation (Morrow and Cooper, 2012). relatively small but in some cases plasmids are compa- The analysis of gene gains and losses shows that rable in size to the chromosome, like the megaplasmid about 60% of gene families in the Burkholderia genus in Rhizobium tropici (Geniaux et al., 1995). has experienced horizontal gene transfer. More than The distinction between plasmids and chromosomes 7,000 candidate donors belong to the Proteobacteria is not clearly defined, a fundamental criterion being phylum (Zhu et al., 2011). Gene gains and losses im- that a chromosome must harbor genes essential for pact the pathogenicity of species. The loss of a T3SS- viability. In addition, chromosomes differ from plas- encoding fragment in B. mallei ATCC 23344, compared mids in the replication process. The chromosomal repli- to B. mallei SAVP1, is responsible for the difference in cation is restricted to a particular phase of the cell the virulence between these strains (Schutzer et al., cycle and the origins may be initiated only once per 2008). Another example is the loss of the L-arabinose cycle (Boye, Løbner-Olesen, and Skarstad, 2000). In assimilation operon by pathogens B. mallei and B. pseu- contrast, the plasmid replication is not linked to the domallei in comparison with an avirulent strain B. thai- cell cycle (Leonard and Helmstetter, 1988) and may landensis. Introducing the L-arabinose assimilation be initiated several times per cycle (Solar et al., 1998). operon in a B. pseudomallei strain made it less viru- However, some replicons carry essential genes but have lent (Moore et al., 2004). Hence, although the mech- plasmid-like replication systems (Egan, Fogel, and Wal- anism is not clear, there must be a link between the dor, 2005), and it is not obvious how to classify them. presence of this operon and virulence. Gene loss also Recently, the term “chromid” has been proposed for influences the adaptability of an organism. The ge- such replicons (Harrison et al., 2010). nomic reduction of B. mallei following its divergence We analyzed bacteria from the genus Burkholderia. from B. pseudomallei likely resulted in its inability to Their genomes are comprised of two or three chro- live outside the host (Losada et al., 2010; Godoy et al., mosomes. The genus is ecologically diverse (Coenye 2003). The acquisition of the atrazine degradation and and Vandamme, 2003); for example, B. mallei and nitrotoluene degradation pathways by B. glumae PG1, B. pseudomallei are pathogens causing glanders and compared to B. glumae LMG 2196 and B. glumae BGR1, melioidosis, respectively, in human and animals (Howe, could result from an adaption since these toxic agents Sampath, and Spotnitz, 1971); B. glumae is a pathogen are used in the farming industry as a herbicide and a of rice (Ham, Melanson, and Rush, 2011); B. xen- pesticide, respectively (Lee et al., 2016). ovorans is an effective degrader of polychlorinated B. pseudomallei is known to have a high rate of biphenyl, used
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