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Comparative Genomic and Metabolic Analysis of Three Lactobacillus

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Comparative Genomic and Metabolic Analysis of Three Lactobacillus Stefanovic and McAuliffe BMC Genomics (2018)19:205 https://doi.org/10.1186/s12864-018-4586-0 RESEARCH ARTICLE Open Access Comparative genomic and metabolic analysis of three Lactobacillus paracasei cheese isolates reveals considerable genomic differences in strains from the same niche Ewelina Stefanovic* and Olivia McAuliffe Abstract Background: Strains of Lactobacillus paracasei are present in many diverse environments, including dairy and plant materials and the intestinal tracts of humans and animals. Their adaptation to various niches is correlated to intra-species diversity at the genomic and metabolic level. In this study, we compared the genome sequences of three L. paracasei strains isolated from mature Cheddar cheeses, two of which (DPC4206 and DPC4536) shared the same genomic fingerprint by PFGE, but demonstrated varying metabolic capabilities. Results: Genome sizes varied from 2.9 Mbp for DPC2071, to 3.09 Mbp for DPC4206 and 3.08 Mpb for DPC4536. The presence of plasmids was a distinguishing feature between the strains with strain DPC2071 possessing an unusually high number of plasmids (up to 11), while DPC4206 had one plasmid and DPC4536 harboured no plasmids. Each of the strains possessed specific genes not present in the other two analysed strains. The three strains differed in their abundance of sugar-converting genes, and in the types of sugars that could be used as energy sources. Genes involved in the metabolism of sugars not usually connected with the dairy niche, such as myo-inositol and pullulan were also detected, but strains did not utilise these sugars. The genetic content of the three strains differed in regard to specific genes for arginine and sulfur-containing amino acid metabolism and genes contributing to resistance to heavy metal ions. In addition, variability in the presence of phage remnants and phage protection systems was evident. Conclusions: The findings presented in this study confirm a considerable level of heterogeneity of Lactobacillus paracasei strains, even between strains isolated from the same niche. Keywords: Lactobacillus paracasei, comparative genomics, dairy Background and Lactobacillus rhamnosus. Strains of this group show The genus Lactobacillus consists of more than 200 species remarkable ecological adaptability and have been isolated and subspecies [1] present in various environments such from all the typical habitats of lactobacilli [4, 5]. Such a as plants, fermented food products (dairy, meat, wine), diverse range of sources facilitated a broad spectrum of and both the human and animal gastrointestinal and re- applications of strains of this species in dairy production productive tracts [2, 3]. One of the most studied groups of (adjunct cultures), and in health-related (probiotics, bacte- this genus is the Lactobacillus casei group, which includes riocins) and biotechnological fields. These characteristics the species Lactobacillus casei, Lactobacillus paracasei and potential applications make the species of the L. casei group one of the best explored within the Lactobacillus * Correspondence: [email protected] genus. Department of Food Biosciences, Teagasc Food Research Centre, Moorepark, Fermoy, Ireland © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Stefanovic and McAuliffe BMC Genomics (2018)19:205 Page 2 of 13 To date, the genome sequences of 118 L. casei and L. profiles, despite demonstrating considerable differences in paracasei strains are publicly available, 21 of which are selected enzyme activities, such as cell envelope protein- complete genome sequences (http://www.ncbi.nlm.nih.- ase, aminopeptidases, aminotransferase and glutamate de- gov, last accessed in January 2018). The comparative hydrogenase [12]. Similarly, these two strains exhibited genomic analysis of L. casei and L. paracasei genomes distinct differences when examined for the production of has revealed that, as in other Lactobacillales, there is an volatile flavour compounds in two cheese model systems evolutionary trend towards minimisation of genome size [13]. The third strain (DPC2071), which differed consider- through the decay of genes coding for functions not ably in its PFGE profile, possessed high levels of activity of required for strains inhabiting specific niches. This loss enzymes of the proteolytic system, especially cell envelope of redundant genes has been shown to be followed by proteinase, and exhibited one of the most distinct volatile the acquisition of genes by horizontal gene transfer profiles in cheese model systems [12, 13]. It was proposed (HGT) as a response to niche adaptation [6]. The rich that elucidation and comparison of the genomes of these pool of available genome sequences enables the defin- three strains would enhance our understanding of the ition of the gene sets that are common to all strains genetic basis of their different phenotypic characteristics. (core genome), the genes present in only some of the strains (dispensable genome), or genes that are unique for a single strain (unique genes). Insights into the com- Methods mon and unique genes enable correlation of gene varia- Bacterial strains for comparative analysis tions among different strains to the presence or absence The three L. paracasei strainsexaminedinthisstudywere of phenotypic traits [7]. The pangenome (or supragen- isolated from the non-starter microbiota of Cheddar cheese, ome) comprises the union of all genes present within a and deposited in the DPC Culture Collection. The genomes selected genome set (species, genera or higher taxo- of all three strains are available from public databases nomic group) [8]. L. casei and L. paracasei pangenome (accession numbers: NCSN01000000, NCSO01000000 and studies have confirmed the wide range of ecological NCSP01000000, for strains DPC2071, DPC4206 and niches that can be inhabited by strains of the L. casei DPC4536, respectively). Details of genome sequencing and group [4, 7, 9], arising from the variability of genes assembly were previously reported [14]. Contig mapping supporting utilisation of numerous energy sources and was performed using Mauve, with the genomes of L. other specific genes contributing to efficient survival in paracasei ATCC 334, L. casei BDII and L. casei 12A as habitats with differing environmental conditions. references for strains DPC2071, DPC4206 and DPC4536, The dairy niche represents a nutritionally rich habitat, respectively [15]. and niche specialisation in dairy strains has led to sub- stantial gene decay, which has limited their survival in more nutritionally scarce environments [5]. As a conse- Identification of strain-specific genes in each of the input quence, genomes of dairy isolates possess a higher ratio genomes of pseudogenes, compared to non-dairy isolates [10]. Whole genome comparisons were undertaken using Conversely, genomes of dairy specialists are abundant BLAST Ring Image Generator [16], and progressive- in sugar transportation, proteolytic and amino acid Mauve alignments [15], in order to identify unique transportation-encoding genes that enable uptake of genomic regions belonging to each of the strains. nutrients present in the dairy environment [6]. However, Clustered regularly interspaced short palindromic the isolation source does not necessarily correspond to repeat (CRISPR) regions in each genome were identified the original niche in which a strain has evolved, as strains using an online tool CRISPRfinder [17]. Viable and cryp- can change their habitats due to their adaptability. This is tic prophages within each of the genomes were detected evident from genome content, where often unusual genes using PHASTER tool [18]. Contigs representing plasmid that are not expected for strains from a specific niche are sequences were predicted based on the presence of typical present, suggesting that a strain may have transferred plasmid-associated genes, such as replication and mobil- from one niche to another [11]. isation genes, or based on similarity to sequences of previ- The aim of this study was to compare the genomic and ously published plasmids (www.ncbi.nlm.nih.gov). metabolic characteristics of three L. paracasei strains that were isolated from mature Cheddar cheeses. Previously, these strains were selected based on the activity of the key Plasmid profiles enzymes involved in flavour production and their volatile Plasmid DNA was isolated using a method previously profiles in cheese model systems [12, 13]. Genomic described [19]. Plasmid DNA was run on a 0.7 % (w/v) fingerprinting established that two of the strains agarose gel, and visualised by staining with ethidium (DPC4206 and DPC4536) showed identical PFGE bromide. Stefanovic and McAuliffe BMC Genomics (2018)19:205 Page 3 of 13 Modified media to assess carbohydrate fermentation Determination of antibiotic resistance profiles Modified MRS broth (MMRS) was made by the omission To determine the strains’ resistance to antibiotics, of beef extract and any other additional sugar source
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