Comparative genomics of the lactic acid bacteria

K Makarova

A Slesarev

Y Wolf

A Sorokin

V Karamychev+41 authors

^{National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894;}

^{Fidelity Systems Inc., 7961 Cessna Avenue, Gaithersburg, MD 20879;}

^{School of Information Systems and Computer Science, Birkbeck College, University of London, Malet Street, London WC1E 7HX, United Kingdom;}

^{U.S. Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598;}

^{Department of Food Science, North Carolina State University, Raleigh, NC 27695;}

^{North Carolina Agricultural Research Service, U.S. Department of Agriculture, Raleigh, NC 27695; Departments of}

^{Biology and}

^{Nutrition and Food Science and}

^{Center for Integrated BioSystems, Utah State University, Logan, UT 84322;}

^{Department of Food Science and Technology, University of Nebraska, Lincoln, NE 68583;}

^{Department of Food Science and Nutrition, University of Minnesota, St. Paul, MN 55108;}

^{Department of Food Science, University of Wisconsin, Madison, WI 53706;}

^{Department of Biology, University of California at San Diego, La Jolla, CA 92093;}

^{Department of Viticulture and Enology, University of California, Davis, CA 95616; and}

^{Department of Food Science and Toxicology, University of Idaho, Moscow, ID 83844}

^{To whom correspondence may be addressed. E-mail:}vog.hin.mln.ibcn@ninook, ude.uscn.ytinu@krt, ude.usu.cc@remiewcb, or ude.sivadcu@sllimad

Contributed by T. Klaenhammer, August 16, 2006

Author contributions: A. Slesarev, E.K., T.H., F.B., J.B., R.H., D.O., J.S., G.U., M.S., T.K., P.R., S.K., B.W., and D.M. designed research; K.M., A. Slesarev, A. Sorokin, B.M., A.P., N. Pavlova, V.K., N. Polouchine, V. Shakhova, I.G., Y.L., S.L., K.H., D.M.G., V.P., D.W., J.H., Y.G., K.B., J.-H.L., I.D.-M., B.D., V. Smeianov, W.W., R. Barabote, G.L., E.A., R. Barrangou, B.G., Y.X., H.R., D.T., C.P., and S.K. performed research; A.P., N. Pavlova, N. Polouchine, B.G., Y.X., and S.K. contributed new reagents/analytic tools; A. Slesarev, Y.W., A.P., V.K., I.G., D.R., A.B., G.L., E.A., R. Barrangou, F.B., J.B., R.H., D.O., J.S., G.U., M.S., T.K., P.R., S.K., B.W., and D.M. analyzed data; and K.M., Y.W., E.K., T.K., P.R., S.K., and D.M. wrote the paper.

^{Present addresses for K.H., T.H., V.P., I.D.-M., W.W., G.L., E.A., R. Barrangou, Y.X., H.R., D.T., and C.P. are published as supporting information on the PNAS web site.}

Abstract

Lactic acid-producing bacteria are associated with various plant and animal niches and play a key role in the production of fermented foods and beverages. We report nine genome sequences representing the phylogenetic and functional diversity of these bacteria. The small genomes of lactic acid bacteria encode a broad repertoire of transporters for efficient carbon and nitrogen acquisition from the nutritionally rich environments they inhabit and reflect a limited range of biosynthetic capabilities that indicate both prototrophic and auxotrophic strains. Phylogenetic analyses, comparison of gene content across the group, and reconstruction of ancestral gene sets indicate a combination of extensive gene loss and key gene acquisitions via horizontal gene transfer during the coevolution of lactic acid bacteria with their habitats.

Keywords: evolutionary genomics, fermentation

Abstract

Lactic acid bacteria (LAB) are historically defined as a group of microaerophilic, Gram-positive organisms that ferment hexose sugars to produce primarily lactic acid. This functional classification includes a variety of industrially important genera, including Lactococcus, Enterococcus, Oenococcus, Pediococcus, Streptococcus, Leuconostoc, and Lactobacillus species. The seemingly simplistic metabolism of LAB has been exploited throughout history for the preservation of foods and beverages in nearly all societies dating back to the origins of agriculture (1). Domestication of LAB strains passed down through various culinary traditions and continuous passage on food stuffs has resulted in modern-day cultures able to carry out these fermentations. Today, LAB play a prominent role in the world food supply, performing the main bioconversions in fermented dairy products, meats, and vegetables. LAB also are critical for the production of wine, coffee, silage, cocoa, sourdough, and numerous indigenous food fermentations (2).

LAB species are indigenous to food-related habitats, including plant (fruits, vegetables, and cereal grains) and milk environments. In addition, LAB are naturally associated with the mucosal surfaces of animals, e.g., small intestine, colon, and vagina. Isolates of the same species often are obtained from plant, dairy, and animal habitats, implying wide distribution and specialized adaptation to these diverse environments. LAB species employ two pathways to metabolize hexose: a homofermentative pathway in which lactic acid is the primary product and a heterofermentative pathway in which lactic acid, CO₂, acetic acid, and/or ethanol are produced (3).

Complete genome sequences have been published for eight fermentative and commensal LAB species: Lactococcus lactis, Lactobacillus plantarum, Lactobacillus johnsonii, Lactobacillus acidophilus, Lactobacillus sakei, Lactobacillus bulgaricus, Lactobacillus salivarius, and Streptococcusthermophilus (4 –11). This study examines nine other LAB genomes representing the phylogenetic and functional diversity of lactic acid-producing microorganisms. The LAB have small genomes encoding a range of biosynthetic capabilities that reflect both prototrophic and auxotrophic characters. Phylogenetic analyses, comparison of genomic content across the group, and reconstruction of ancestral gene sets reveal a combination of gene loss and gain during the coevolution of LAB with animals and the foods they consumed.

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Acknowledgments

We dedicate this work to the career and many contributions of Prof. Larry McKay, a pioneering researcher on the genetics of lactic acid bacteria. This work was supported by the Intramural Program of the National Library of Medicine; the U.S. Department of Energy Office of Science, Biological, and Environmental Research Program and the University of California, Lawrence Livermore National Laboratory under Contract W-7405-Eng-48; the Lawrence Berkeley National Laboratory under Contract DE-AC03-76SF00098l; and the Los Alamos National Laboratory under Contract W-7405-ENG-36. Genome closure was supported by Department of Energy Small Business Innovative Research Grants DE-FG02-98ER82577 and DE-FG02-00ER83009 (to A. Slesarev and S.K.). Additional funding came from the American Vineyard Foundation (to D.M.); the California Competitive Grants Program for Research in Viticulture and Enology (to D.M.); the Western Dairy Center (to B.W.); the Utah Agricultural Experiment Station (to B.W.); Dairy Management, Inc. (to B.W., T.K., and D.O.); Danisco, Inc. (to T.K.); the Southeast Dairy Foods Research Center (to T.K.); the North Carolina Dairy Foundation (to T.K.); the North Carolina Agricultural Research Service (to T.K.); National Institutes of Health Grant R01 GM55434 (to M.S.); the U.S. Department of Agriculture Agricultural Research Service Food Science Research Unit (to F.B.); Pickle Packers International, Inc. (to F.B.); the Utah State Community University Research Initiative (to J.B.); the Nebraska American Dairy Association (to R.H.); Minnesota Agriculture Experiment Station Project 18-062 (to K.B.); the Minnesota–South Dakota Dairy Foods Research Center (to D.O.); and the University of Wisconsin College of Agriculuture and Life Science (to J.S.).

Acknowledgments

Abbreviations

LAB	lactic acid bacteria
COG	cluster of orthologous genes
LaCOG	Lactobacillales-specific COG
HGT	horizontal gene transfer

Abbreviations

Footnotes

The authors declare no conflict of interest.

Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. {"type":"entrez-nucleotide","attrs":{"text":"CP000411","term_id":"116090851","term_text":"CP000411"}}CP000411–{"type":"entrez-nucleotide","attrs":{"text":"CP000430","term_id":"116109013","term_text":"CP000430"}}CP000430).

Footnotes

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