Bifidobacterium asteroides PRL2011 Genome Analysis Reveals Clues for Colonization of the Insect Gut

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Bottacini, Francesca ^a   Milani, Christian ^b   Turroni, Francesca ^a   Sánchez, Borja ^c   Foroni, Elena ^b   Duranti, Sabrina ^b   Serafini, Fausta ^b   Viappiani, Alice ^b   Strati, Francesco ^b   Ferrarini, Alberto ^d   Delledonne, Massimo ^d   Henrissat, Bernard ^e   Coutinho, Pedro ^e   Fitzgerald, Gerald F ^a   Margolles, Abelardo ^c   van Sinderen, Douwe ^a   Ventura, Marco ^b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY OF PARMA   (Italy)

^c DEPARTMENT OF MICROBIOLOGY AND BIOCHEMISTRY OF DAIRY PRODUCTS   (Spain)

^d UNIVERSITY OF VERONA   (Italy)

^e AIX MARSEILLE UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

OXYGEN;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM ISOLATE; BIFIDOBACTERIUM; BIFIDOBACTERIUM ASTEROIDES; CONTROLLED STUDY; DNA BASE COMPOSITION; EVOLUTIONARY ADAPTATION; GENE CLUSTER; GENE FUNCTION; GENE SEQUENCE; GENETIC CONSERVATION; GENOME ANALYSIS; GENOMICS; HONEYBEE; INTESTINE; MICROBIAL RESPIRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRL2011 GENE; SEQUENCE HOMOLOGY;

ANIMALS; BIFIDOBACTERIUM; CLUSTER ANALYSIS; GASTROINTESTINAL TRACT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE ORDER; GENETIC VARIATION; GENOME, BACTERIAL; INSECTS; OXYGEN CONSUMPTION; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

ANIMALIA; APIS MELLIFERA; BIFIDOBACTERIUM; BIFIDOBACTERIUM ASTEROIDES; HEXAPODA; MAMMALIA;

EID: 84866673240     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044229     Document Type: Article

References (80)

1. Fanning S, Hall LJ, Cronin M, Zomer A, Macsharry J, et al. (2012) Bifidobacterial surface-exopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection. Proc Natl Acad Sci U S A 109: 2108-2113.
2. Macfarlane S, Bahrami B, Macfarlane GT, (2011) Mucosal biofilm communities in the human intestinal tract. Adv Appl Microbiol 75: 111-143.
3. Hooper LV, Gordon JI, (2001) Commensal host-bacterial relationships in the gut. Science 292: 1115-1118.
4. Ouwehand AC, Salminen S, Isolauri E, (2002) Probiotics: an overview of beneficial effects. Antonie Van Leeuwenhoek 82: 279-289.
5. Guarner F, Malagelada JR, (2003) Gut flora in health and disease. Lancet 361: 512-519.
6. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI, (2005) Host-bacterial mutualism in the human intestine. Science 307: 1915-1920.
7. Saxelin M, Tynkkynen S, Mattila-Sandholm T, de Vos WM, (2005) Probiotic and other functional microbes: from markets to mechanisms. Curr Opin Biotechnol 16: 204-211.
8. Marco ML, Pavan S, Kleerebezem M, (2006) Towards understanding molecular modes of probiotic action. Curr Opin Biotechnol 17: 204-210.
9. Killer J, Kopecny J, Mrazek J, Koppova I, Havlik J, et al. (2011) Bifidobacterium actinocoloniiforme sp. nov. and Bifidobacterium bohemicum sp. nov., from the bumblebee digestive tract. Int J Syst Evol Microbiol 61: 1315-1321.
10. Scardovi V, Trovatelli LD, (1969) New species of bifid bacteria from Apis mellifica L. and Apis indica F. A contribution to the taxonomy and biochemistry of the genus Bifidobacterium. Zentralbl Bakteriol Parasitenkd Infektionskr Hyg 123: 64-88.
11. Killer J, Kopecny J, Mrazek J, Rada V, Dubna S, et al. (2010) Bifidobacteria in the digestive tract of bumblebees. Anaerobe 16: 165-170.
12. Jeyaprakash A, Hoy MA, Allsopp MH, (2003) Bacterial diversity in worker adults of Apis mellifera capensis and Apis mellifera scutellata (Insecta: Hymenoptera) assessed using 16S rRNA sequences. J Invertebr Pathol 84: 96-103.
13. Mrazek J, Strosova L, Fliegerova K, Kott T, Kopecny J, (2008) Diversity of insect intestinal microflora. Folia Microbiol (Praha) 53: 229-233.
14. Turroni F, van Sinderen D, Ventura M, (2011) Genomics and ecological overview of the genus Bifidobacterium. Int J Food Microbiol 149: 37-44.
15. Ventura M, Canchaya C, Tauch A, Chandra G, Fitzgerald GF, et al. (2007) Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol Mol Biol Rev 71: 495-548.
16. Baughn AD, Malamy MH, (2004) The strict anaerobe Bacteroides fragilis grows in and benefits from nanomolar concentrations of oxygen. Nature 427: 441-444.
17. Jones SA, Chowdhury FZ, Fabich AJ, Anderson A, Schreiner DM, et al. (2007) Respiration of Escherichia coli in the mouse intestine. Infect Immun 75: 4891-4899.
18. Simpson PJ, Stanton C, Fitzgerald GF, Ross RP, (2005) Intrinsic tolerance of Bifidobacterium species to heat and oxygen and survival following spray drying and storage. J Appl Microbiol 99: 493-501.
19. Mozzetti V, Grattepanche F, Moine D, Berger B, Rezzonico E, et al. (2010) New method for selection of hydrogen peroxide adapted bifidobacteria cells using continuous culture and immobilized cell technology. Microb Cell Fact 9: 60.
20. Shimamura S, Abe F, Ishibashi N, Miyakawa H, Yaeshima T, et al. (1992) Relationship between oxygen sensitivity and oxygen metabolism of Bifidobacterium species. J Dairy Sci 75: 3296-3306.
21. Meile L, Ludwig W, Rueger U, Gut C, Kaufmann P, et al. (1997) Bifidobacterium lactis sp. nov, a moderately oxygen tolerant species isolated from fermented milk. Systematic and Applied Microbiology 20: 57-64.
22. Simpson PJ, Ross RP, Fitzgerald GF, Stanton C, (2004) Bifidobacterium psychraerophilum sp nov and Aeriscardovia aeriphila gen. nov., sp nov., isolated from a porcine caecum. International Journal of Systematic and Evolutionary Microbiology 54: 401-406.
23. Kawasaki S, Mimura T, Satoh T, Takeda K, Niimura Y, (2006) Response of the microaerophilic Bifidobacterium species, B. boum and B. thermophilum, to oxygen. Appl Environ Microbiol 72: 6854-6858.
24. Turroni F, Bottacini F, Foroni E, Mulder I, Kim JH, et al. (2010) Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging. Proc Natl Acad Sci U S A 107: 19514-19519.
25. Ventura M, Turroni F, Zomer A, Foroni E, Giubellini V, et al. (2009) The Bifidobacterium dentium Bd1 genome sequence reflects its genetic adaptation to the human oral cavity. PLoS Genet 5: e1000785.
26. Kim JF, Jeong H, Yu DS, Choi SH, Hur CG, et al. (2009) Genome sequence of the probiotic bacterium Bifidobacterium animalis subsp. lactis AD011. J Bacteriol 191: 678-679.
27. Barrangou R, Briczinski EP, Traeger LL, Loquasto JR, Richards M, et al. (2009) Comparison of the complete genome sequences of Bifidobacterium animalis subsp. lactis DSM 10140 and Bl-04. J Bacteriol 191: 4144-4151.
28. Sela DA, Chapman J, Adeuya A, Kim JH, Chen F, et al. (2008) The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc Natl Acad Sci U S A 105: 18964-18969.
29. Schell MA, Karmirantzou M, Snel B, Vilanova D, Berger B, et al. (2002) The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc Natl Acad Sci U S A 99: 14422-14427.
30. O'Connell Motherway M, Zomer A, Leahy SC, Reunanen J, Bottacini F, et al. (2011) Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. Proc Natl Acad Sci U S A 108: 11217-11222.
31. Paoli M, (2001) Protein folds propelled by diversity. Prog Biophys Mol Biol 76: 103-130.
32. Stevens TJ, Paoli M, (2008) RCC1-like repeat proteins: a pangenomic, structurally diverse new superfamily of beta-propeller domains. Proteins 70: 378-387.
33. Lim D, Park HU, De Castro L, Kang SG, Lee HS, et al. (2001) Crystal structure and kinetic analysis of beta-lactamase inhibitor protein-II in complex with TEM-1 beta-lactamase. Nat Struct Biol 8: 848-852.
34. Yeoman CJ, Yildirim S, Thomas SM, Durkin AS, Torralba M, et al. (2010) Comparative genomics of Gardnerella vaginalis strains reveals substantial differences in metabolic and virulence potential. PLoS One 5: e12411.
35. Creevey CJ, Muller J, Doerks T, Thompson JD, Arendt D, et al. (2011) Identifying single copy orthologs in Metazoa. PLoS Comput Biol 7: e1002269.
36. de Vries W, Stouthamer AH, (1969) Factors determining the degree of anaerobiosis of Bifidobacterium strains. Arch Mikrobiol 65: 275-287.
37. Mills DA, Rawsthorne H, Parker C, Tamir D, Makarova K, (2005) Genomic analysis of Oenococcus oeni PSU-1 and its relevance to winemaking. FEMS Microbiol Rev 29: 465-475.
38. Lemme A, Sztajer H, Wagner-Dobler I, (2010) Characterization of mleR, a positive regulator of malolactic fermentation and part of the acid tolerance response in Streptococcus mutans. BMC Microbiol 10: 58.
39. Brokl M, Soria AC, Ruiz-Matute AI, Sanz ML, Ramos L, (2010) Separation of disaccharides by comprehensive two-dimensional gas chromatography-time-of-flight mass spectrometry. Application to honey analysis. J Agric Food Chem 58: 11561-11567.
40. Saier MH Jr, Yen MR, Noto K, Tamang DG, Elkan C, (2009) The Transporter Classification Database: recent advances. Nucleic Acids Res 37: D274-278.
41. Lee JH, Karamychev VN, Kozyavkin SA, Mills D, Pavlov AR, et al. (2008) Comparative genomic analysis of the gut bacterium Bifidobacterium longum reveals loci susceptible to deletion during pure culture growth. BMC Genomics 9: 247.
42. van den Broek LA, Hinz SW, Beldman G, Vincken JP, Voragen AG, (2008) Bifidobacterium carbohydrases-their role in breakdown and synthesis of (potential) prebiotics. Mol Nutr Food Res 52: 146-163.
43. Pokusaeva K, Fitzgerald GF, van Sinderen D, (2011) Carbohydrate metabolism in Bifidobacteria. Genes Nutr 6: 285-306.
44. Unden G, Bongaerts J, (1997) Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors. Biochim Biophys Acta 1320: 217-234.
45. Ingledew WJ, Poole RK, (1984) The respiratory chains of Escherichia coli. Microbiol Rev 48: 222-271.
46. Cotter PA, Chepuri V, Gennis RB, Gunsalus RP, (1990) Cytochrome o (cyoABCDE) and d (cydAB) oxidase gene expression in Escherichia coli is regulated by oxygen, pH, and the fnr gene product. J Bacteriol 172: 6333-6338.
47. Winstedt L, Yoshida K, Fujita Y, von Wachenfeldt C, (1998) Cytochrome bd biosynthesis in Bacillus subtilis: characterization of the cydABCD operon. J Bacteriol 180: 6571-6580.
48. Gunsalus RP, Brusilow WS, Simoni RD, (1982) Gene order and gene-polypeptide relationships of the proton-translocating ATPase operon (unc) of Escherichia coli. Proc Natl Acad Sci U S A 79: 320-324.
49. Kasimoglu E, Park SJ, Malek J, Tseng CP, Gunsalus RP, (1996) Transcriptional regulation of the proton-translocating ATPase (atpIBEFHAGDC) operon of Escherichia coli: control by cell growth rate. J Bacteriol 178: 5563-5567.
50. Ventura M, Canchaya C, Zink R, Fitzgerald GF, van Sinderen D, (2004) Characterization of the groEL and groES loci in Bifidobacterium breve UCC 2003: genetic, transcriptional, and phylogenetic analyses. Appl Environ Microbiol 70: 6197-6209.
51. Bott M, Niebisch A, (2003) The respiratory chain of Corynebacterium glutamicum. J Biotechnol 104: 129-153.
52. Schryvers A, Lohmeier E, Weiner JH, (1978) Chemical and functional properties of the native and reconstituted forms of the membrane-bound, aerobic glycerol-3-phosphate dehydrogenase of Escherichia coli. J Biol Chem 253: 783-788.
53. Mcgavin GC, (1994) The Insects- an Outline of Entomology- Gullan,Pj, Cranston,Ps. Nature 370: 261-262.
54. Govantes F, Albrecht JA, Gunsalus RP, (2000) Oxygen regulation of the Escherichia coli cytochrome d oxidase (cydAB) operon: roles of multiple promoters and the Fnr-1 and Fnr-2 binding sites. Mol Microbiol 37: 1456-1469.
55. Duwat P, Sourice S, Cesselin B, Lamberet G, Vido K, et al. (2001) Respiration capacity of the fermenting bacterium Lactococcus lactis and its positive effects on growth and survival. J Bacteriol 183: 4509-4516.
56. Pedersen MB, Garrigues C, Tuphile K, Brun C, Vido K, et al. (2008) Impact of aeration and heme-activated respiration on Lactococcus lactis gene expression: identification of a heme-responsive operon. J Bacteriol 190: 4903-4911.
57. Kakinuma Y, Igarashi K, (1994) Purification and characterization of the catalytic moiety of vacuolar-type Na(+)-ATPase from Enterococcus hirae. J Biochem 116: 1302-1308.
58. Yokota A, Veenstra M, Kurdi P, van Veen HW, Konings WN, (2000) Cholate resistance in Lactococcus lactis is mediated by an ATP-dependent multispecific organic anion transporter. J Bacteriol 182: 5196-5201.
59. Breckau D, Mahlitz E, Sauerwald A, Layer G, Jahn D, (2003) Oxygen-dependent coproporphyrinogen III oxidase (HemF) from Escherichia coli is stimulated by manganese. J Biol Chem 278: 46625-46631.
60. Sanchez B, de los Reyes-Gavilan CG, Margolles A, (2006) The F1F0-ATPase of Bifidobacterium animalis is involved in bile tolerance. Environ Microbiol 8: 1825-1833.
61. Matsumoto M, Ohishi H, Benno Y, (2004) H+-ATPase activity in Bifidobacterium with special reference to acid tolerance. Int J Food Microbiol 93: 109-113.
62. Shi L, Sohaskey CD, Kana BD, Dawes S, North RJ, et al. (2005) Changes in energy metabolism of Mycobacterium tuberculosis in mouse lung and under in vitro conditions affecting aerobic respiration. Proc Natl Acad Sci U S A 102: 15629-15634.
63. Ventura M, Canchaya C, Del Casale A, Dellaglio F, Neviani E, et al. (2006) Analysis of bifidobacterial evolution using a multilocus approach. Int J Syst Evol Microbiol 56: 2783-2792.
64. Ventura M, Turroni F, O'Connell Motherway M, MacSharry J, van Sinderen D, (2012) Host-microbe interactions that facilitate gut colonization by commensal bifidobacteria. Trends in Microbiology In Press.
65. Imlay JA, (2003) Pathways of oxidative damage. Annu Rev Microbiol 57: 395-418.
66. Ventura M, Elli M, Reniero R, Zink R, (2001) Molecular microbial analysis of Bifidobacterium isolates from different environments by the species-specific amplified ribosomal DNA restriction analysis (ARDRA). FEMS Microbiol Ecol 36: 113-121.
67. Sambrook J, Russel DW (2001) Molecular cloning a laboratory manual (3rd ed.) Cold Spring Harbor Laboratory Press, New York. 435 p.
68. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
69. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, et al. (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11: 119.
70. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, et al. (2000) Artemis: sequence visualization and annotation. Bioinformatics 16: 944-945.
71. Lowe TM, Eddy SR, (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: 955-964.
72. Volfovsky N, Haas BJ, Salzberg SL, (2001) A clustering method for repeat analysis in DNA sequences. Genome Biol 2: RESEARCH0027.
73. Coutinho PM, Henrissat B, (1999) Life with no sugars? J Mol Microbiol Biotechnol 1: 307-308.
74. Busch W, Saier MH Jr, (2002) The transporter classification (TC) system, 2002. Crit Rev Biochem Mol Biol 37: 287-337.
75. Gao F, Zhang CT, (2006) GC-Profile: a web-based tool for visualizing and analyzing the variation of GC content in genomic sequences. Nucleic Acids Res 34: W686-691.
76. Bilban M, Buehler LK, Head S, Desoye G, Quaranta V, (2002) Defining signal thresholds in DNA microarrays: exemplary application for invasive cancer. BMC Genomics 3: 19.
77. Bolstad BM, Irizarry RA, Astrand M, Speed TP, (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193.
78. Eisen MB, Spellman PT, Brown PO, Botstein D, (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95: 14863-14868.
79. Turroni F, Foroni E, Pizzetti P, Giubellini V, Ribbera A, et al. (2009) Exploring the diversity of the bifidobacterial population in the human intestinal tract. Appl Environ Microbiol 75: 1534-1545.
80. Rouillard JM, Zuker M, Gulari E, (2003) OligoArray 2.0: design of oligonucleotide probes for DNA microarrays using a thermodynamic approach. Nucleic Acids Res 31: 3057-3062.