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Genomic reconstruction of transcriptional regulatory networks in lactic acid bacteria.

ABSTRACT: BACKGROUND: Genome scale annotation of regulatory interactions and reconstruction of regulatory networks are the crucial problems in bacterial genomics. The Lactobacillales order of bacteria collates various microorganisms having a large economic impact, including both human and animal pathogens and strains used in the food industry. Nonetheless, no systematic genome-wide analysis of transcriptional regulation has been previously made for this taxonomic group. RESULTS: A comparative genomics approach was used for reconstruction of transcriptional regulatory networks in 30 selected genomes of lactic acid bacteria. The inferred networks comprise regulons for 102 orthologous transcription factors (TFs), including 47 novel regulons for previously uncharacterized TFs. Numerous differences between regulatory networks of the Streptococcaceae and Lactobacillaceae groups were described on several levels. The two groups are characterized by substantially different sets of TFs encoded in their genomes. Content of the inferred regulons and structure of their cognate TF binding motifs differ for many orthologous TFs between the two groups. Multiple cases of non-orthologous displacements of TFs that control specific metabolic pathways were reported. CONCLUSIONS: The reconstructed regulatory networks substantially expand the existing knowledge of transcriptional regulation in lactic acid bacteria. In each of 30 studied genomes the obtained regulatory network contains on average 36 TFs and 250 target genes that are mostly involved in carbohydrate metabolism, stress response, metal homeostasis and amino acids biosynthesis. The inferred networks can be used for genetic experiments, functional annotations of genes, metabolic reconstruction and evolutionary analysis. All reconstructed regulons are captured within the Streptococcaceae and Lactobacillaceae collections in the RegPrecise database (http://regprecise.lbl.gov).

SUBMITTER: Ravcheev DA

PROVIDER: S-EPMC3616900 | biostudies-other | 2013

REPOSITORIES: biostudies-other

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Genomic reconstruction of transcriptional regulatory networks in lactic acid bacteria.

Ravcheev Dmitry A DA Best Aaron A AA Sernova Natalia V NV Kazanov Marat D MD Novichkov Pavel S PS Rodionov Dmitry A DA

BMC genomics 20130212

<h4>Background</h4>Genome scale annotation of regulatory interactions and reconstruction of regulatory networks are the crucial problems in bacterial genomics. The Lactobacillales order of bacteria collates various microorganisms having a large economic impact, including both human and animal pathogens and strains used in the food industry. Nonetheless, no systematic genome-wide analysis of transcriptional regulation has been previously made for this taxonomic group.<h4>Results</h4>A comparative ...[more]

PMID: 23398941

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Project description:BackgroundLactic acid bacteria (LAB) are important in the food industry for the production of fermented food products and in human health as commensals in the gut. However, the phylogenetic relationships among LAB species remain under intensive debate owing to disagreements among different data sets.ResultsWe performed a phylogenetic analysis of LAB species based on 232 genes from 28 LAB genome sequences. Regardless of the tree-building methods used, combined analyses yielded an identical, well-resolved tree topology with strong supports for all nodes. The LAB species examined were divided into two groups. Group 1 included families Enterococcaceae and Streptococcaceae. Group 2 included families Lactobacillaceae and Leuconostocaceae. Within Group 2, the LAB species were divided into two clades. One clade comprised of the acidophilus complex of genus Lactobacillus and two other species, Lb. sakei and Lb. casei. In the acidophilus complex, Lb. delbrueckii separated first, while Lb. acidophilus/Lb. helveticus and Lb. gasseri/Lb. johnsonii were clustered into a sister group. The other clade within Group 2 consisted of the salivarius subgroup, including five species, Lb. salivarius, Lb. plantarum, Lb. brevis, Lb. reuteri, Lb. fermentum, and the genera Pediococcus, Oenococcus, and Leuconostoc. In this clade, Lb. salivarius was positioned most basally, followed by two clusters, one corresponding to Lb. plantarum/Lb. brevis pair and Pediococcus, and the other including Oenococcus/Leuconostoc pair and Lb. reuteri/Lb. fermentum pair. In addition, phylogenetic utility of the 232 genes was analyzed to identify those that may be more useful than others. The genes identified as useful were related to translation and ribosomal structure and biogenesis (TRSB), and a three-gene set comprising genes encoding ultra-violet resistance protein B (uvrB), DNA polymerase III (polC) and penicillin binding protein 2B (pbpB).ConclusionsOur phylogenomic analyses provide important insights into the evolution and diversification of LAB species, and also revealed the phylogenetic utility of several genes. We infer that the occurrence of multiple, independent adaptation events in LAB species, have resulted in their occupation of various habitats. Further analyses of more genes from additional, representative LAB species are needed to reveal the molecular mechanisms underlying adaptation of LAB species to various environmental niches.

Project description:BACKGROUND: Lactic acid bacteria (LAB) are a group of gram-positive, lactic acid producing Firmicutes. They have been extensively used in food fermentations, including the production of various dairy products. The proteolytic system of LAB converts proteins to peptides and then to amino acids, which is essential for bacterial growth and also contributes significantly to flavor compounds as end-products. Recent developments in high-throughput genome sequencing and comparative genomics hybridization arrays provide us with opportunities to explore the diversity of the proteolytic system in various LAB strains. RESULTS: We performed a genome-wide comparative genomics analysis of proteolytic system components, including cell-wall bound proteinase, peptide transporters and peptidases, in 22 sequenced LAB strains. The peptidase families PepP/PepQ/PepM, PepD and PepI/PepR/PepL are described as examples of our in silico approach to refine the distinction of subfamilies with different enzymatic activities. Comparison of protein 3D structures of proline peptidases PepI/PepR/PepL and esterase A allowed identification of a conserved core structure, which was then used to improve phylogenetic analysis and functional annotation within this protein superfamily.The diversity of proteolytic system components in 39 Lactococcus lactis strains was explored using pangenome comparative genome hybridization analysis. Variations were observed in the proteinase PrtP and its maturation protein PrtM, in one of the Opp transport systems and in several peptidases between strains from different Lactococcus subspecies or from different origin. CONCLUSIONS: The improved functional annotation of the proteolytic system components provides an excellent framework for future experimental validations of predicted enzymatic activities. The genome sequence data can be coupled to other "omics" data e.g. transcriptomics and metabolomics for prediction of proteolytic and flavor-forming potential of LAB strains. Such an integrated approach can be used to tune the strain selection process in food fermentations.

Dataset Information

Genomic reconstruction of transcriptional regulatory networks in lactic acid bacteria.

Publications

Genomic reconstruction of transcriptional regulatory networks in lactic acid bacteria.

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