Nomadic lifestyle of <i>Lactobacillus plantarum</i> revealed by comparative genomics of 54 strains isolated from different habitats

Martino, Maria Elena; Bayjanov, Jumamurat R.; Caffrey, Brian E.; Wels, Michiel; Joncour, Pauline; Hughes, Sandrine; Gillet, Benjamin; Kleerebezem, Michiel; Hijum, Sacha A. F. T. van; Leulier, François

doi:10.1111/1462-2920.13455

Cited by 182 publications

(194 citation statements)

References 65 publications

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“…This has been adopted in a study of Lactobacillus plantarum , which is prevalent in both the guts of animals, including Drosophila, and other habitats. Interestingly, the genomic content of L. plantarum is uncoupled from source of isolation (Martino et al., ), paralleling our conclusions for Acetobacter . A second strategy would be to address among‐strain variation in regulation of gene expression.…”

Section: Discussionsupporting

confidence: 86%

A genomic investigation of ecological differentiation between free‐living and Drosophila‐associated bacteria

et al. 2017

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Various bacterial taxa have been identified both in association with animals and in the external environment, but the extent to which related bacteria from the two habitat types are ecologically and evolutionarily distinct is largely unknown. This study investigated the scale and pattern of genetic differentiation between bacteria of the family Acetobacteraceae isolated from the guts of Drosophila fruit flies, plant material and industrial fermentations. Genome-scale analysis of the phylogenetic relationships and predicted functions was conducted on 44 Acetobacteraceae isolates, including newly-sequenced genomes from 18 isolates from wild and laboratory Drosophila. Isolates from the external environment and Drosophila could not be assigned to distinct phylogenetic groups, nor are their genomes enriched for any different sets of genes or category of predicted gene functions. In contrast, analysis of bacteria from laboratory Drosophila showed they were genetically distinct in their universal capacity to degrade uric acid (a major nitrogenous waste product of Drosophila) and absence of flagellar motility, while these traits vary among wild Drosophila isolates. Analysis of the competitive fitness of Acetobacter discordant for these traits revealed a significant fitness deficit for bacteria that cannot degrade uric acid in culture with Drosophila. We propose that, for wild populations, frequent cycling of Acetobacter between Drosophila and the external environment prevents genetic differentiation by maintaining selection for traits adaptive in both the gut and external habitats. However, laboratory isolates bear the signs of adaptation to persistent association with the Drosophila host under tightly-defined environmental conditions.

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Section: Discussionsupporting

confidence: 86%

A genomic investigation of ecological differentiation between free‐living and Drosophila‐associated bacteria

et al. 2017

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“…Interestingly, all known specialized LAB Streptococcus thermophilus, L. iners, L. reuteri, L. sanfranciscensis , and L. fructivorans are characterized by a small secretome, suggesting that colonizing one specific niche, such as dairy, vagina, sourdough, or the GI tract, respectively, does not require a large secretome. Consistently, the known generalist LAB such as L. rhamnosus, L. plantarum (Martino et al, 2016), and some Enterococcus spp. exhibit a large secretome.…”

Section: Resultsmentioning

confidence: 73%

Comparative Genomic Analysis Reveals Ecological Differentiation in the Genus Carnobacterium

et al. 2017

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Lactic acid bacteria (LAB) differ in their ability to colonize food and animal-associated habitats: while some species are specialized and colonize a limited number of habitats, other are generalist and are able to colonize multiple animal-linked habitats. In the current study, Carnobacterium was used as a model genus to elucidate the genetic basis of these colonization differences. Analyses of 16S rRNA gene meta-barcoding data showed that C. maltaromaticum followed by C. divergens are the most prevalent species in foods derived from animals (meat, fish, dairy products), and in the gut. According to phylogenetic analyses, these two animal-adapted species belong to one of two deeply branched lineages. The second lineage contains species isolated from habitats where contact with animal is rare. Genome analyses revealed that members of the animal-adapted lineage harbor a larger secretome than members of the other lineage. The predicted cell-surface proteome is highly diversified in C. maltaromaticum and C. divergens with genes involved in adaptation to the animal milieu such as those encoding biopolymer hydrolytic enzymes, a heme uptake system, and biopolymer-binding adhesins. These species also exhibit genes for gut adaptation and respiration. In contrast, Carnobacterium species belonging to the second lineage encode a poorly diversified cell-surface proteome, lack genes for gut adaptation and are unable to respire. These results shed light on the important genomics traits required for adaptation to animal-linked habitats in generalist Carnobacterium.

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“…This diversity explains the capability of the Lactobacillus species to colonize extremely different habitats. Together with freeliving species, niche/ecosystem specialists populate specific habitats (e.g., dairy products or vertebrate gastrointestinal tracts), while generalists adapt to a variety of different environments (Martino et al, 2016). Lactobacillus plantarum is one of the best examples of generalist species.…”

Section: Introductionmentioning

confidence: 99%

“…AFLP and RAPD-PCR (Kleerebezem et al, 2003;Frese et al, 2011;Siezen and van Hylckama Vlieg, 2011;Sun et al, 2015), multilocus sequence typing (Sun et al, 2015) and microarraybased comparative genome hybridization (Molenaar et al, 2005) have been the most common approaches used. Two main conclusions seem to emerge, the high genomic diversity that imparts metabolic flexibility (Molenaar et al, 2005;Siezen et al, 2010a;Frese et al, 2011), and the typical nomadic lifestyle (Martino et al, 2016). Indeed, L. plantarum has acquired and retained functional capabilities, which confer a dynamic and flexible behaviour (Duar et al, 2014;He et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

“…This is an open ecosystem, which, inevitably, suffers by contamination from food matrices and their viable microbes. Besides, the isolation of a strain from a particular habitat does not always reflect strain colonization of that environment but mostly a free-living status (Martino et al, 2016). Although genetic markers explaining the environmental adaptation of L. plantarum are unknown, the second issue concerns the relatively scarce knowledge on regulatory mechanisms such as gene expression.…”

Section: Introductionmentioning

confidence: 99%

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How Lactobacillus plantarum shapes its transcriptome in response to contrasting habitats

Filannino

Angelis

Cagno

et al. 2018

Environmental Microbiology

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Triplets of Lactobacullus plantarum strains were isolated from nine contrasting habitats. Without any passage through other culture media, isolation and cultivation were on model media that strictly reproduced the chemical and physical conditions and stressors of the habitats of origin. Here, we demonstrated how L. plantarum regulates and shapes its transcriptome in response to contrasting habitats. Firstly, multivariate clustering analysis of transcriptional data (RNA-Seq), complemented with metabolomics and phenomics, grouped the strains according to the habitats of origin. Subsequently, selected strains from each habitat switched to repeated cultivation on MRS medium and transcriptomes homogenized into a unique cluster. Adaptation to this common medium mainly relied on activation of genes for phage- and prophage-related proteins and transposases. Finally, the comparison of growth across model media and with respect to MRS medium showed that 44% of the overall 3112 gene transcripts changed depending on the specific habitat. Regulation and shaping of transcriptomes mainly concerned carbohydrate acquisition, pyruvate catabolism, proteolytic system and amino acid, lipid and inorganic ion transport and metabolism, with contrasting responses for contrasting habitats. Pathways reconstruction demonstrated how the large genome size of L. plantarum imparts transcriptome and metabolic flexibility as the basic mechanism for a nomadic lifestyle.

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Nomadic lifestyle of Lactobacillus plantarum revealed by comparative genomics of 54 strains isolated from different habitats

Cited by 182 publications

References 65 publications

A genomic investigation of ecological differentiation between free‐living and Drosophila‐associated bacteria

A genomic investigation of ecological differentiation between free‐living and Drosophila‐associated bacteria

Comparative Genomic Analysis Reveals Ecological Differentiation in the Genus Carnobacterium

How Lactobacillus plantarum shapes its transcriptome in response to contrasting habitats

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