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  • Review Article
  • Published:

Genome-scale analyses of health-promoting bacteria: probiogenomics

Nature Reviews Microbiology volume 7, pages 61–71 (2009)Cite this article

Key Points

  • The human gastrointestinal tract (GIT) is a complex ecosystem, the bacterial components (microbiota) of which are thought to have a significant role in normal gut function and in maintaining host health. The human gut microbiota include health-promoting indigenous species such as Bifidobacterium and Lactobacillus, also referred to as probiotic bacteria. Probiotic bacteria are commonly consumed live as dietary supplements.

  • The molecular mechanisms by which probiotic bacteria exert their health-promoting effects remain largely unclear. However, the advent of a novel scientific discipline, called probiogenomics, has recently provided new insights into the diversity and evolution of probiotic bacteria and has revealed the molecular basis of probiosis.

  • Probiogenomic efforts have shown how the genome content of bifidobacteria and lactobacilli reflect adaptations to the human intestinal niche. Genomic evidence for adaptations to the GIT includes metabolic features, such as the capacity for uptake of macromolecules and breakdown of undigested complex carbohydrates, and the ability to interact with the host through the production of cell-surface proteins that interact with the intestinal mucosa.

  • The interaction of probiotic bacteria with the host, as well as with other components of the human gut microbiota, is considered a key feature of probiosis. Bifidobacteria inducean expansion in the diversity of polysaccharides that are targeted for degradation by common intestinal bacteria (Bacteroides) and also inducethe expression of host genes that play a part in innate immunity.

  • Comparisons among completely sequenced bifidobacterial and lactobacilli genomes revealed that the main force that drives evolution in these genomes is horizontal gene transfer.

  • Probiotic bacteria are diverse and taxonomically heterogeneous groups of microorganisms, so the analysis of phyletic patterns — that is, patterns of gene presence or absence in a particular set of genomes — might be influenced by the evolutionary distance between these distant phyla. Nevertheless, comparative analyses of genomes from probiotic bacteria revealed a core genome (probiogenome), which encodes key functions of this group of microorganisms.

Abstract

The human body is colonized by an enormous population of bacteria (microbiota) that provides the host with coding capacity and metabolic activities. Among the human gut microbiota are health-promoting indigenous species (probiotic bacteria) that are commonly consumed as live dietary supplements. Recent genomics-based studies (probiogenomics) are starting to provide insights into how probiotic bacteria sense and adapt to the gastrointestinal tract environment. In this Review, we discuss the application of probiogenomics in the elucidation of the molecular basis of probiosis using the well-recognized model probiotic bacteria genera Bifidobacterium and Lactobacillus as examples.

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Figure 1: Evolutionary relationships between the main gastrointestinal tract commensal bacterial groups.
Figure 2: Acquisition of sugars by bifidobacteria.
Figure 3: Comparative analysis of Bifidobacterium genomes.
Figure 4: Comparative analysis of Lactobacillus genomes.

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Acknowledgements

Work in the laboratories of D.v.S. and P.W.O.T. is supported by a Science Foundation Ireland Centres for Science, Engineering & Technology (SFI CSET) award to the Alimentary Pharmabiotic Centre and a Department of Agriculture and Food (DAF)/Health Research Board, Food-Health Research Initiative (HRB FHRI) FHRI award to the ELDERMET project. M.V. was supported by an Italian Award for Outstanding Young Researcher scheme “Incentivazione alla mobilità di studiosi stranieri e italiani residente all'estero” 2005–2009, a Marie Curie Reintegration Grant (MERG-CT-2005-03,080) and Parmalat spa, Italy. We also thank C. Canchaya for helpful discussions. Work on genomics of lactobacilli at North Carolina State University, USA, is supported by the NC Dairy Foundation, Danisco USA Inc. and Dairy Management Inc.

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Authors and Affiliations

  1. Department of Genetics, Biology of Microorganisms, Anthropology and Evolution, University of Parma, 43100, Italy

    Marco Ventura & Francesca Turroni

  2. Department of Food, Bioprocessing and Nutrition Sciences, North Carolina State University, Raleigh, 27695, North Carolina, USA

    Sarah O'Flaherty & Todd R. Klaenhammer

  3. Alimentary Pharmabiotic Centre and Department of Microbiology, University College Cork, Western Road, Cork, Ireland

    Marcus J. Claesson, Douwe van Sinderen & Paul W. O'Toole

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  1. Marco Ventura
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Correspondence to Paul W. O'Toole.

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DATABASES

Entrez Genome Project

Bacteroides thetaiotaomicron

Bifidobacterium adolescentis

Bifidobacterium breve

Bifidobacterium dentium

Bifidobacterium longum

Enterococcus faecium

Escherichia coli

Lactobacillus acidophilus

Lactobacillus delbrueckii

Lactobacillus fermentum

Lactobacillus gasseri

Lactobacillus helveticus

Lactobacillus johnsonii

Lactobacillus plantarum

Lactobacillus reuteri

Lactobacillus rhamnosus

Lactobacillus salivarius

Lactococcus lactis

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Alimentary Pharmabiotic Centre

ELDERMET

Univeristy of Parma

Glossary

Microbiota

The collective microbial community or population that resides in a particular locale at a given time.

Phylotypes

Groups of bacteria that are defined by percentage identity in their 16S rRNA gene sequences.

Neighbour-joining tree

A tree that reconstructs the evolutionary development of organisms on the basis of distances between pairs of taxa.

Omics

The integration of genomics methodology and data with functional genomic analyses involving transcriptomics, proteomics, metabolomics and interactomics.

Prebiotics

Growth substrates that are preferentially (or ideally, exclusively) metabolized by a single genus or species and that may thus be used as dietary supplements to promote growth of a targeted health-promoting microorganism.

Transcriptome

The subset of genes that are transcribed in an organism. It represents dynamic links between a genome, proteins and cellular phenotypes.

Synteny

Genetic linkage or conservation of gene order.

Bacteriocins

Proteinaceous substances that are produced by one bacterium to kill another bacterium, usually by inducing leakage or lysis. Bacteriocins are composed of one or two short peptides that can be post-translationally modified.

COGs

Clusters of orthologous groups are delineated by comparing protein sequences that are encoded in complete genomes, representing major phylogenetic lineages. Each COG consists of individual proteins or groups of paralogues from at least 3 lineages and thus corresponds to an ancient conserved domain.

Autochthonous

Members of the microbiota that are growing where they are found, as distinct from transient species that are only passing through the environment.

Pseudoparalogous

An extra copy of a gene that is already present in a genome that was acquired by lateral gene transfer rather than by gene duplication.

Microbiome

The collective genome of microbial communities.

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Ventura, M., O'Flaherty, S., Claesson, M. et al. Genome-scale analyses of health-promoting bacteria: probiogenomics. Nat Rev Microbiol 7, 61–71 (2009). https://doi.org/10.1038/nrmicro2047

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