Probing the pan-genome of Listeria monocytogenes: new insights into intraspecific niche expansion and genomic diversification

Deng, Xiangyu; Phillippy, Adam M.; Li, Zengxin; Salzberg, Steven L.; Zhang, Wei

doi:10.1186/1471-2164-11-500

Cited by 82 publications

(90 citation statements)

References 84 publications

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“…The number of genes unique to a single strain ranged from 22 to 117, and various subclades within PE15 also had unique genes. As expected (33,47), many of the most newly acquired unique genes reflected the comings and goings of phage and transposons ( Fig. 2A).…”

Section: Discussionsupporting

confidence: 69%

“…In addition, genome content differences between the closest relatives must be shown to have ecological importance. Genome content differences among members of the same species are dominated by genes that are functional for phage or transposons and by the so-called "hypothetical" genes, with no known function for bacteria (33,47). An ecologically motivated genome comparison should do more than track the comings and goings of genetic elements that parasitize bacteria.…”

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confidence: 99%

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Genomic Heterogeneity and Ecological Speciation within One Subspecies of Bacillus subtilis

Kopac

Wang

Wiedenbeck

et al. 2014

Appl Environ Microbiol

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bClosely related bacterial genomes usually differ in gene content, suggesting that nearly every strain in nature may be ecologically unique. We have tested this hypothesis by sequencing the genomes of extremely close relatives within a recognized taxon and analyzing the genomes for evidence of ecological distinctness. We compared the genomes of four Death Valley isolates plus the laboratory strain W23, all previously classified as Bacillus subtilis subsp. spizizenii and hypothesized through multilocus analysis to be members of the same ecotype (an ecologically homogeneous population), named putative ecotype 15 (PE15). These strains showed a history of positive selection on amino acid sequences in 38 genes. Each of the strains was under a different regimen of positive selection, suggesting that each strain is ecologically unique and represents a distinct ecological speciation event. The rate of speciation appears to be much faster than can be resolved with multilocus sequencing. Each PE15 strain contained unique genes known to confer a function for bacteria. Remarkably, no unique gene conferred a metabolic system or subsystem function that was not already present in all the PE15 strains sampled. Thus, the origin of ecotypes within this clade shows no evidence of qualitative divergence in the set of resources utilized. Ecotype formation within this clade is consistent with the nanoniche model of bacterial speciation, in which ecotypes use the same set of resources but in different proportions, and genetic cohesion extends beyond a single ecotype to the set of ecotypes utilizing the same resources.

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Section: Discussionsupporting

confidence: 69%

mentioning

confidence: 99%

Genomic Heterogeneity and Ecological Speciation within One Subspecies of Bacillus subtilis

Kopac

Wang

Wiedenbeck

et al. 2014

Appl Environ Microbiol

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“…Lmo0753 is a putative Crp/Fnr transcriptional regulator that shares two similar functional domains with PrfA, the master virulence regulator in L. monocytogenes (8). The shared functional domains are an N-terminally located cofactor binding domain and a C-terminally located helix-turn-helix domain consisting of two ␣-helices that are capable of resting in the major groove in DNA (9).…”

Section: Discussionmentioning

confidence: 99%

“…Previously reported human listeriosis outbreaks were predominantly caused by LI and LII strains, but rarely by strains in the LIII group (1). In our previous study, we conducted pangenomic analysis of 26 L. monocytogenes strains, including eight from LIII (8). We identified 86 disparately distributed genes (DDGs) and eight noncoding small RNAs that were highly conserved in LI and LII genomes but absent in LIII genomes.…”

mentioning

confidence: 99%

prfA -Like Transcription Factor Gene lmo0753 Contributes to l -Rhamnose Utilization in Listeria monocytogenes Strains Associated with Human Food-Borne Infections

Salazar

McMullen

et al. 2013

Appl Environ Microbiol

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e Listeria monocytogenes is a food-borne bacterial pathogen and the causative agent of human and animal listeriosis. Among the three major genetic lineages of L. monocytogenes (i.e., LI, LII, and LIII), LI and LII are predominantly associated with food-borne listeriosis outbreaks, whereas LIII is rarely implicated in human infections. In a previous study, we identified a Crp/Fnr family transcription factor gene, lmo0753, that was highly specific to outbreak-associated LI and LII but absent from LIII. Lmo0753 shares two conserved functional domains, including a DNA binding domain, with the well-characterized master virulence regulator PrfA in L. monocytogenes. In this study, we constructed lmo0753 deletion and complementation mutants in two fully sequenced L. monocytogenes LII strains, 10403S and EGDe, and compared the flagellar motility, phospholipase C production, hemolysis, and intracellular growth of the mutants and their respective wild types. Our results suggested that lmo0753 plays a role in hemolytic activity in both EGDe and 10403S. More interestingly, we found that deletion of lmo0753 led to the loss of L-rhamnose utilization in EGDe, but not in 10403S. RNA-seq analysis of EGDe ⌬0753 incubated in phenol red medium containing L-rhamnose as the sole carbon source revealed that 126 (4.5%) and 546 (19.5%) out of 2,798 genes in the EGDe genome were up-and downregulated more than 2-fold, respectively, compared to the wild-type strain. Genes related to biotin biosynthesis, general stress response, and rhamnose metabolism were shown to be differentially regulated. Findings from this study collectively suggested varied functional roles of lmo0753 in different LII L. monocytogenes strain backgrounds associated with human listeriosis outbreaks.

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“…In addition, the comparative genomic analyses was able to identify genomic changes associated with differences in specific taxa (Binnewies et al 2006;Cho et al 2010;Deng et al 2010), as seen in this study between grazed alone and co-grazed animals. …”

Section: High Throughput Studies Of Microbial Habitatmentioning

confidence: 80%

The biochemical and microbiological characteristics of rumen fluid from cattle co-grazed with and without camels as compared to that from the foregut of camels

Suyub¹

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Co-grazing is a common practice under many range conditions. The main advantage of co-grazing is to fully utilize the vegetation sources by taking advantage of the different preferences among animals towards plant species and parts. Hence, this study aimed to establish if co-grazing camels with cattle would lead to changes in the biochemical characteristics in the rumen contents of cattle, and result in different fermentation end products. Rumen contents were collected from two groups of animals at two different locations, the Runnymede Cattle Station at Richmond in northern Queensland, and the Meramist abattoir at Caboolture in Queensland. For the Richmond site, two groups of animals were sampled via stomach tube; cattle co-grazed with camels (n=6) and cattle grazed alone (n=6). For the Caboolture site, foregut contents from three groups of animals were sampled post mortem; camels co-grazed with cattle (n=6), cattle cograzed with camels (n=6), and camels grazed alone (n=6). The ratios of camel to cattle for the Richmond and the Caboolture sites were 1:49 and 1:14 respectively. These ratios were considered adequate for microbial transfer to occur.Foregut fluid samples from all animals were used to inoculate a pre-reduced medium containing Mitchell grass (Astrebla lappacea), Flinders grass (Iseilema spp.), or Lucerne hay (Medicago sativa). Measurements of gas production, volatile fatty acids, and dry matter digestibility were carried out following 48 or 96 h of in vitro incubation at 39 °C.Inocula from cattle co-grazed with camels from Richmond resulted in greater (P< 0.05) dry matter digestibility for Mitchell grass than cattle grazed alone and produced greater (P< 0.05) amounts of n-butyrate. On the other hand, inocula of camels co-grazed with cattle from Caboolture had higher in vitro dry matter digestibility for Mitchell grass and shared the potential for higher dry matter digestibility with cattle co-grazed with camels for lucerne hay. Camels co-grazed with cattle also produced more (P<0.05) n-Butyric acid in the Mitchell grass treatment compared to groups of camels grazed alone and cattle co-grazed with camels. The results from the biochemical analysis suggested that co-grazing may change the ecosystem of the foregut in a number of beneficial ways.A microbiological analysis was carried out to investigate the structure of the bacterial community in each group of animals with high throughput sequencing of 16s rRNA gene using 454 pyrosequencing technology. Using an open source software computational program provided by Quantitative Insights into Microbial Ecology (QIIME), not only was it possible to identify all microbial species within the foregut fluid samples but also it was possible for all data to be analysed and compared systematically.Further analyses to identify the different operational taxonomic units (OTUs) with a similarity threshold of 97% allowed the assessment of observed species (OTUs); species richness (Chao1); and phylogenetic diversity (PD) whole tree metric for each foregut fluid sa...

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Probing the pan-genome of Listeria monocytogenes: new insights into intraspecific niche expansion and genomic diversification

Cited by 82 publications

References 84 publications

Genomic Heterogeneity and Ecological Speciation within One Subspecies of Bacillus subtilis

Genomic Heterogeneity and Ecological Speciation within One Subspecies of Bacillus subtilis

prfA -Like Transcription Factor Gene lmo0753 Contributes to l -Rhamnose Utilization in Listeria monocytogenes Strains Associated with Human Food-Borne Infections

The biochemical and microbiological characteristics of rumen fluid from cattle co-grazed with and without camels as compared to that from the foregut of camels

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