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.

Continue Reading

Data Availability

Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. CP000411–CP000430).

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.).

Supporting Information

Adobe PDF - 07117Fig4.pdf
Adobe PDF - 07117Fig4.pdf
Adobe PDF - 07117Fig5.pdf
Adobe PDF - 07117Fig5.pdf
Adobe PDF - 07117Fig6.pdf
Adobe PDF - 07117Fig6.pdf
Adobe PDF - 07117Fig7.pdf
Adobe PDF - 07117Fig7.pdf
Adobe PDF - 07117Fig8.pdf
Adobe PDF - 07117Fig8.pdf
07117Table2.xls
07117Table3.xls
07117Table4.xls
07117Table5.xls
07117Table6.xls
07117Table7.xls
07117Table8.xls
07117Table1.doc

References

1
N Miller, W Wetterstrom The Cambridge World History of Food, eds K Kiple, K Ornelas (Cambridge Univ Press, Cambridge, UK) Vol 2, 1123–1139 (2000).
2
B Wood Microbiology of Fermented Foods (Blackie, London, 1998).
3
O Kandler Antonie van Leeuwenhoek 49, 209–224 (1983).
4
E Altermann, W Russell, M Azcarate-Peril, R Barrangou, B Buck, O McAuliffe, N Souther, A Dobson, T Duong, M Callanan, et al. Proc Natl Acad Sci USA 102, 3906–3912 (2005).
5
A Bolotin, B Quinquis, P Renault, A Sorokin, S Ehrlich, S Kulakauskas, A Lapidus, E Goltsman, M Mazur, G Pusch, et al. Nat Biotechnol 22, 1554–1558 (2004).
6
A Bolotin, P Wincker, S Mauger, O Jaillon, K Malarme, J Weissenbach, S Ehrlich, A Sorokin Genome Res 11, 731–753 (2001).
7
S Chaillou, M Champomier-Verges, M Cornet, A Crutz-Le Coq, AM Dudez, V Martin, S Beaufils, E Darbon-Rongere, R Bossy, V Loux, M Zagorec Nat Biotechnol 23, 1527–1533 (2005).
8
M Kleerebezem, J Boekhorst, R van Kranenburg, D Molenaar, OP Kuipers, R Leer, R Tarchini, S Peters, H Sandbrink, M Fiers, et al. Proc Natl Acad Sci USA 100, 1990–1995 (2003).
9
R Pridmore, B Berger, F Desiere, D Vilanova, C Barretto, A Pittet, M Zwahlen, M Rouvet, E Altermann, R Barrangou, et al. Proc Natl Acad Sci USA 101, 2512–2517 (2004).
10
M Claesson, Y Li, S Leahy, C Canchaya, J van Pijkeren, A Cerdeno-Tarraga, J Parkhill, S Flynn, G O'Sullivan, J Collins, et al. Proc Natl Acad Sci USA 103, 6718–6723 (2006).
11
M van de Guchte, S Penaud, C Grimaldi, V Barbe, K Bryson, P Nicolas, C Robert, S Oztas, S Mangenot, A Couloux, et al. Proc Natl Acad Sci USA 103, 9274–9279 (2006).
12
J Klappenbach, J Dunbar, T Schmidt Appl Environ Microbiol 66, 1328–1333 (2000).
13
E Di Mattia, S Grego, I Cacciari Microb Ecol 43, 34–43 (2002).
14
L McKay, K Baldwin FEMS Microbiol Rev 7, 3–14 (1990).
15
P Vandamme, B Pot, M Gillis, P de Vos, K Kersters, J Swings Microbiol Rev 60, 407–438 (1996).
16
B Wood, W Holzapfel The Genera of Lactic Acid Bacteria (Blackie, Glasgow, UK, 1995).
17
Y Wolf, I Rogozin, N Grishin, R Tatusov, E Koonin BMC Evol Biol 1, 8 (2001).
18
R Siezen, F van Enckevort, M Kleerebezem, B Teusink Curr Opin Biotechnol 15, 105–115 (2004).
19
N Takezaki, A Rzhetsky, M Nei Mol Biol Evol 12, 823–833 (1995).
20
D Yang, C Woese Syst Appl Microbiol 12, 145–149 (1989).
21
I Jordan, I Rogozin, Y Wolf, E Koonin Theor Popul Biol 61, 435–447 (2002).
22
M Lynch, J Conery Science 302, 1401–1404 (2003).
23
R Tatusov, E Koonin, D Lipman Science 278, 631–637 (1997).
24
R Tatusov, N Fedorova, J Jackson, A Jacobs, B Kiryutin, E Koonin, D Krylov, R Mazumder, S Mekhedov, A Nikolskaya, et al. BMC Bioinformatics 4, 41 (2003).
25
R Leipuviene, Q Qian, G Bjork J Bacteriol 186, 758–766 (2004).
26
P Novichkov, M Omelchenko, M Gelfand, A Mironov, Y Wolf, E Koonin J Bacteriol 186, 6575–6585 (2004).
27
B Wood, P Warner Genetics of Lactic Acid Bacteria (Kluwer Academic/Plenum, New York, 2003).
28
R Siezen, B Renckens, I van Swam, S Peters, R van Kranenburg, M Kleerebezem, W de Vos Appl Environ Microbiol 71, 8371–8382 (2005).
29
B Mirkin, T Fenner, M Galperin, E Koonin BMC Evol Biol 3, 2 (2003).
30
J Hastings, W Holzapfel, J Niemand Appl Environ Microbiol 52, 898–901 (1986).
31
M Horsburgh, S Wharton, M Karavolos, S Foster Trends Microbiol 10, 496–501 (2002).
32
M Daly, E Gaidamakova, V Matrosova, A Vasilenko, M Zhai, A Venkateswaran, M Hess, M Omelchenko, H Kostandarithes, KS Makarova, et al. Science 306, 1025–1028 (2004).
33
F Archibald, I Fridovich J Bacteriol 145, 442–451 (1981).
34
Y Li, J Hugenholtz, T Abee, D Molenaar Appl Environ Microbiol 69, 5739–5745 (2003).
35
H Ochman Proc Natl Acad Sci USA 102, 11959–11960 (2005).
36
I Jordan, K Makarova, J Spouge, Y Wolf, E Koonin Genome Res 11, 555–565 (2001).
37
E Koonin, K Makarova, L Aravind Annu Rev Microbiol 55, 709–742 (2001).
38
E Jamet, S Ehrlich, F Duperray, P Renault Lait 81, 115–129 (2001).
39
A Katla, H Kruse, G Johnsen, H Herikstad Int J Food Microbiol 67, 147–152 (2001).
40
M Teuber, L Meile, F Schwarz Antonie van Leeuwenhoek 76, 115–137 (1999).
41
C Yeats, RD Finn, A Bateman Trends Biochem Sci 27, 438 (2002).
42
H Nishi, H Komatsuzawa, T Fujiwara, N McCallum, M Sugai Antimicrob Agents Chemother 48, 4800–4807 (2004).
43
B Snel, P Bork, M Huynen Genome Res 12, 17–25 (2002).
44
Y Wolf, I Rogozin, A Kondrashov, E Koonin Genome Res 11, 356–372 (2001).
45
E Koonin, M Galperin Sequence–Evolution–Function: Computational Approaches in Comparative Genomics (Kluwer Academic, London, 2003).
46
D Hemme, C Foucaud-Scheunemann Int Dairy J 14, 467–494 (2004).
47
S-Q Liu Int J Food Microbiol 83, 115–131 (2003).
48
D Twomey, R Ross, M Ryan, B Meaney, C Hill Antonie van Leeuwenhoek 82, 165–185 (2002).
49
I Nes, O Johnsborg Curr Opin Biotechnol 15, 100–104 (2004).
50
A Metivier, M Pilet, X Dousset, O Sorokine, P Anglade, M Zagorec, JC Piard, D Marion, Y Cenatiempo, C Fremaux Microbiology 144, 2837–2844 (1998).
51
S Aparicio, J Chapman, E Stupka, N Putnam, J Chia, P Dehal, A Christoffels, S Rash, S Hoon, A Smit, et al. Science 297, 1301–1310 (2002).
52
A Slesarev, K Mezhevaya, K Makarova, N Polushin, O Shcherbinina, V Shakhova, G Belova, L Aravind, D Natale, I Rogozin, et al. Proc Natl Acad Sci USA 99, 4644–4649 (2002).
53
J Besemer, A Lomsadze, M Borodovsky Nucleic Acids Res 29, 2607–2618 (2001).
54
S Altschul, T Madden, A Schaffer, J Zhang, Z Zhang, W Miller, D Lipman Nucleic Acids Res 25, 3389–3402 (1997).
55
T Lowe, S Eddy Nucleic Acids Res 25, 955–964 (1997).
56
R Tatusov, D Natale, I Garkavtsev, T Tatusova, U Shankavaram, BS Rao, B Kiryutin, M Galperin, N Fedorova, E Koonin Nucleic Acids Res 29, 22–28 (2001).

Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 103 | No. 42
October 17, 2006
PubMed: 17030793

Classifications

Data Availability

Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. CP000411–CP000430).

Submission history

Published online: October 17, 2006
Published in issue: October 17, 2006

Keywords

  1. evolutionary genomics
  2. fermentation

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.).

Authors

Affiliations

K. Makarova
National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894;
A. Slesarev
Fidelity Systems Inc., 7961 Cessna Avenue, Gaithersburg, MD 20879;
Y. Wolf
National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894;
A. Sorokin
National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894;
B. Mirkin
School of Information Systems and Computer Science, Birkbeck College, University of London, Malet Street, London WC1E 7HX, United Kingdom;
National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894;
A. Pavlov
Fidelity Systems Inc., 7961 Cessna Avenue, Gaithersburg, MD 20879;
N. Pavlova
Fidelity Systems Inc., 7961 Cessna Avenue, Gaithersburg, MD 20879;
V. Karamychev
Fidelity Systems Inc., 7961 Cessna Avenue, Gaithersburg, MD 20879;
N. Polouchine
Fidelity Systems Inc., 7961 Cessna Avenue, Gaithersburg, MD 20879;
V. Shakhova
Fidelity Systems Inc., 7961 Cessna Avenue, Gaithersburg, MD 20879;
I. Grigoriev
U.S. Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598;
Y. Lou
U.S. Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598;
D. Rohksar
U.S. Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598;
S. Lucas
U.S. Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598;
K. Huang
U.S. Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598;
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.
D. M. Goodstein
U.S. Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598;
T. Hawkins
U.S. Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598;
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.
V. Plengvidhya
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
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.
Y. Goh
Department of Food Science and Technology, University of Nebraska, Lincoln, NE 68583;
A. Benson
Department of Food Science and Technology, University of Nebraska, Lincoln, NE 68583;
K. Baldwin
Department of Food Science and Nutrition, University of Minnesota, St. Paul, MN 55108;
J.-H. Lee
Department of Food Science and Nutrition, University of Minnesota, St. Paul, MN 55108;
I. Díaz-Muñiz
Department of Food Science, University of Wisconsin, Madison, WI 53706;
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.
B. Dosti
Department of Food Science, University of Wisconsin, Madison, WI 53706;
V. Smeianov
Department of Food Science, University of Wisconsin, Madison, WI 53706;
W. Wechter
Department of Food Science, University of Wisconsin, Madison, WI 53706;
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.
R. Barabote
Department of Biology, University of California at San Diego, La Jolla, CA 92093;
G. Lorca
Department of Biology, University of California at San Diego, La Jolla, CA 92093;
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.
E. Altermann
Department of Food Science, North Carolina State University, Raleigh, NC 27695;
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.
R. Barrangou
Department of Food Science, North Carolina State University, Raleigh, NC 27695;
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.
B. Ganesan
Center for Integrated BioSystems, Utah State University, Logan, UT 84322;
Y. Xie
Nutrition and Food Science and
Center for Integrated BioSystems, Utah State University, Logan, UT 84322;
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.
H. Rawsthorne
Department of Viticulture and Enology, University of California, Davis, CA 95616; and
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.
D. Tamir
National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894;
Department of Viticulture and Enology, University of California, Davis, CA 95616; and
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.
C. Parker
National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894;
Department of Viticulture and Enology, University of California, Davis, CA 95616; and
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.
F. Breidt
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
J. Broadbent
Nutrition and Food Science and
R. Hutkins
Department of Food Science and Technology, University of Nebraska, Lincoln, NE 68583;
D. O'Sullivan
Department of Food Science and Nutrition, University of Minnesota, St. Paul, MN 55108;
J. Steele
Department of Food Science, University of Wisconsin, Madison, WI 53706;
G. Unlu
Department of Food Science and Toxicology, University of Idaho, Moscow, ID 83844
M. Saier
Department of Biology, University of California at San Diego, La Jolla, CA 92093;
T. Klaenhammerd [email protected]
Department of Food Science, North Carolina State University, Raleigh, NC 27695;
P. Richardson
U.S. Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598;
S. Kozyavkin
Fidelity Systems Inc., 7961 Cessna Avenue, Gaithersburg, MD 20879;
Nutrition and Food Science and
Center for Integrated BioSystems, Utah State University, Logan, UT 84322;
Department of Viticulture and Enology, University of California, Davis, CA 95616; and

Notes

d
To whom correspondence may be addressed. E-mail: [email protected], [email protected], [email protected], or [email protected]
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.

Competing Interests

The authors declare no conflict of interest.

Metrics & Citations

Metrics

Note: The article usage is presented with a three- to four-day delay and will update daily once available. Due to ths delay, usage data will not appear immediately following publication. Citation information is sourced from Crossref Cited-by service.


Citation statements

Altmetrics

Citations

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.

Cited by

    Loading...

    View Options

    View options

    PDF format

    Download this article as a PDF file

    DOWNLOAD PDF

    Get Access

    Login options

    Check if you have access through your login credentials or your institution to get full access on this article.

    Personal login Institutional Login

    Recommend to a librarian

    Recommend PNAS to a Librarian

    Purchase options

    Purchase this article to get full access to it.

    Single Article Purchase

    Comparative genomics of the lactic acid bacteria
    Proceedings of the National Academy of Sciences
    • Vol. 103
    • No. 42
    • pp. 15275-15722

    Media

    Figures

    Tables

    Other

    Share

    Share

    Share article link

    Share on social media