Detailed analysis of the microbial population in Malaysian spontaneous cocoa pulp fermentations reveals a core and variable microbiota

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Meersman, Esther ^a,b   Steensels, Jan ^a,b   Mathawan, Melissa ^c   Wittocx, Pieter Jan ^a,b   Saels, Veerle ^a,b   Struyf, Nore ^a,b   Bernaert, Herwig ^c   Vrancken, Gino ^c   Verstrepen, Kevin J ^a,b  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c Barry Callebaut AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA;

ACETOBACTER; ACETOBACTER PASTEURIANUS; ARTICLE; BACTERIAL CELL; BACTERIUM IDENTIFICATION; CACAO; CELL COUNT; CONTROLLED STUDY; DNA SEQUENCE; FERMENTATION TECHNIQUE; FUNGUS IDENTIFICATION; HARVEST PERIOD; LACTOBACILLUS FERMENTUM; MALAYSIA; MICROBIAL DIVERSITY; MICROBIAL POPULATION DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; POPULATION STRUCTURE; SACCHAROMYCES CEREVISIAE;

ACETOBACTER; CACAO; FERMENTATION; LACTOBACILLUS FERMENTUM; MALAYSIA; MICROBIOTA;

EID: 84892903079     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081559     Document Type: Article

References (48)

1. Schwan RF, Wheals AE (2004) The microbiology of cocoa fermentation and its role in chocolate quality. Crit Rev Food Sci Nutr 44: 205-221.
2. Lima LJ, Almeida MH, Nout MJ, Zwietering MH (2011) Theobroma cacao L., "The food of the Gods": quality determinants of commercial cocoa beans, with particular reference to the impact of fermentation. Crit Rev Food Sci Nutr 51: 731-761.
3. Lopez SA, Dimick PS (1995) Cocoa fermentation. In: Reed G, Nagodawithana TW, editors. Biotechnology: Enzymes, Biomass, Food and Feed. 2nd ed. New York: Wiley-VCH. pp. 562-577.
4. Misnawi J, Teguh W (2010) Cocoa chemistry and technology: Lambert Academic Publishing.
5. González SS, Barrio E, Querol A (2007) Molecular identification and characterization of wine yeasts isolated from Tenerife (Canary Island, Spain). J Appl Microbiol 102: 1018-1025.
6. Lopandic K, Tiefenbrunner W, Gangl H, Mandl K, Berger S, et al. (2008) Molecular profiling of yeasts isolated during spontaneous fermentations of Austrian wines. FEMS Yeast Res 8: 1063-1075.
7. Nova MX, Schuler AR, Brasileiro BT, Morais MA, Jr. (2009) Yeast species involved in artisanal cachaca fermentation in three stills with different technological levels in Pernambuco, Brazil. Food Microbiol 26: 460-466.
8. Bokulich NA, Bamforth CW, Mills DA (2012) Brewhouse-resident microbiota are responsible for multi-stage fermentation of American coolship ale. PLoS One 7: e35507.
9. Díaz C, Molina AM, Nähring J, Fischer R (2013) Characterization and dynamic behavior of wild yeast during spontaneous wine fermentation in steel tanks and amphorae. BioMed Research International 2013: 1-13.
10. Ardhana M, Fleet GH (2003) The microbial ecology of cocoa bean fermentations in Indonesia. Int J Food Microbiol 86: 87-99.
11. Jespersen L, Nielsen DS, Honholt S, Jakobsen M (2005) Occurrence and diversity of yeasts involved in fermentation of West African cocoa beans. FEMS Yeast Res 5: 441-453.
12. Nielsen DS, Honholt S, Tano-Debrah K, Jespersen L (2005) Yeast populations associated with Ghanaian cocoa fermentations analysed using denaturing gradient gel electrophoresis (DGGE). Yeast 22: 271-284.
13. Camu N, De Winter T, Verbrugghe K, Cleenwerck I, Vandamme P, et al. (2007) Dynamics and biodiversity of populations of lactic acid bacteria and acetic acid bacteria involved in spontaneous heap fermentation of cocoa beans in Ghana. Appl Environ Microbiol 73: 1809-1824.
14. Nielsen DS, Teniola OD, Ban-Koffi L, Owusu M, Andersson TS, et al. (2007) The microbiology of Ghanaian cocoa fermentations analysed using culture-dependent and culture-independent methods. Int J Food Microbiol 114: 168-186.
15. Camu N, Gonzalez A, De Winter T, Van Schoor A, De Bruyne K, et al. (2008) Influence of turning and environmental contamination on the dynamics of populations of lactic acid and acetic acid bacteria involved in spontaneous cocoa bean heap fermentation in Ghana. Appl Environ Microbiol 74: 86-98.
16. Papalexandratou Z, Vrancken G, De Bruyne K, Vandamme P, De Vuyst L (2011) Spontaneous organic cocoa bean box fermentations in Brazil are characterized by a restricted species diversity of lactic acid bacteria and acetic acid bacteria. Food Microbiol 28: 1326-1338.
17. Papalexandratou Z, Falony G, Romanens E, Jimenez JC, Amores F, et al. (2011) Species diversity, community dynamics, and metabolite kinetics of the microbiota associated with traditional Ecuadorian spontaneous cocoa bean fermentations. Appl Environ Microbiol 77: 7698-7714.
18. Papalexandratou Z, Camu N, Falony G, De Vuyst L (2011) Comparison of the bacterial species diversity of spontaneous cocoa bean fermentations carried out at selected farms in Ivory Coast and Brazil. Food Microbiol 28: 964-973.
19. Cocolin L, Ercolini D (2008) Molecular Techniques in the Microbial Ecology of Fermented Foods; Doyle MP, editor: Springer.
20. Justé A, Thomma BPHJ, Lievens B (2008) Recent advances in molecular techniques to study microbial communities in food-associated matrices and processes. Food Microbiol 25: 745-761.
21. Tristezza M, Vetrano C, Bleve G, Grieco F, Tufariello M, et al. (2012) Autochthonous fermentation starters for the industrial production of Negroamaro wines. J Ind Microbiol Biotechnol 39: 81-92.
22. Illeghems K, De Vuyst L, Papalexandratou Z, Weckx S (2012) Phylogenetic analysis of a spontaneous cocoa bean fermentation metagenome reveals new insights into its bacterial and fungal community diversity. PLoS One 7: e38040.
23. Delmont TO, Robe P, Cecillon S, Clark IM, Constancias F, et al. (2011) Accessing the soil metagenome for studies of microbial diversity. Appl Environ Microbiol 77: 1315-1324.
24. Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, et al. (2012) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Research 41: e1.
25. Bokulich NA, Mills DA (2013) Improved selection of internal transcribed spacer-specific primers enables quantitative, utra-high-throughput profiling of fungal communities. Appl Environ Microbiol 79: 2519-2526.
26. Daniel HM, Vrancken G, Takrama JF, Camu N, De Vos P, et al. (2009) Yeast diversity of Ghanaian cocoa bean heap fermentations. FEMS Yeast Res 9: 774-783.
27. Salminen S, von Wright A, Ouwehand A (2004) Lactic Acid Bacteria: Microbiological and Functional Aspects. New York: CRC Press.
28. Papalexandratou Z, De Vuyst L (2011) Assessment of the yeast species composition of cocoa bean fermentations in different cocoa-producing regions using denaturing gradient gel electrophoresis. FEMS Yeast Res 11: 564-574.
29. Carr JG, Davies PA, Dougan J (1979) Cocoa fermentation in Ghana and Malaysia. London: Tropical Products Institute.
30. Carr JG, Davies PA, Dougan J (1980) Cocoa fermentation in Ghana and Malaysia (part 2): further microbiological methods and results. Bristol: Long Ashton Research Station.
31. Kersters K, Lisdiyanti P, Komagata K, Swings J (2006) The family Acetobacteraceae: the genera Acetobacter, Acidomonas, Asaia, Gluconacetobacter, Gluconobacter and Kozakia. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-M, Stackebrandt E, editors. The prokaryotes. 3rd ed. New York: Springer. pp. 163-200.
32. Gevers D, Huys G, Swings J (2001) Applicability of rep-PCR fingerprinting for identification of Lactobacillus species. FEMS Microbiol Lett 205: 31-36.
33. 5-rep-PCR fingerprinting technique for rapid classification and identification of acetic acid bacteria, with a focus on isolates from Ghanaian fermented cocoa beans. Int J Food Microbiol 125: 79-90.
34. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M, editors. Nucleic acid techniques in bacterial systematics. New York: John Wiley and Sons. pp. 115-175.
35. Turner S, Pryer KM, Miao VPW, Palmer JD (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 46: 327-338.
36. Walter J, Hertel C, Tannock GW, Lis CM, Munro K, et al. (2001) Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Appl Environ Microbiol 67: 2578-2585.
37. Kurtzman CP, Robnett CJ (1997) Identification of clinically important ascomycetous yeasts based on nucleotide divergence in the 5′ end of the large-subunit (26S) ribosomal DNA gene. J Clin Microbiol 35: 1216-1223.
38. Cadez N, Poot GA, Raspor P, Smith MT (2003) Hanseniaspora meyeri sp. nov., Hanseniaspora clermontiae sp. nov., Hanseniaspora lachancei sp. nov. and Hanseniaspora opuntiae sp. nov., novel apiculate yeast species. Int J Syst Evol Microbiol 53: 1671-1680.
39. Daniel HM, Meyer W (2003) Evaluation of ribosomal RNA and actin gene sequences for the identification of ascomycetous yeasts. Int J Food Microbiol 86: 61-78.
40. Tavanti A, Davidson AD, Gow NA, Maiden MC, Odds FC (2005) Candida orthopsilosis and Candida metapsilosis spp. nov. to replace Candida parapsilosis groups II and III. J Clin Microbiol 43: 284-292.
41. Wu ZW, Bai FY (2005) ITS sequence and electrophoretic karyotype comparisons of Candida ethanolica with Pichia deserticola and Candida odintsovae with Pichia rabaulensis. J Gen Appl Microbiol 51: 319-322.
42. Cadez N, Raspor P, Smith MT (2006) Phylogenetic placement of Hanseniaspora-Kloeckera species using multigene sequence analysis with taxonomic implications: descriptions of Hanseniaspora pseudoguilliermondii sp. nov. and Hanseniaspora occidentalis var. citrica var. nov. Int J Syst Evol Microbiol 56: 1157-1165.
43. Lan L, Xu J (2006) Multiple gene genealogical analyses suggest divergence and recent clonal dispersal in the opportunistic human pathogen Candida guilliermondii. Microbiology 152: 1539-1549.
44. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes - application for the identification of mycorrhizae and rusts. Mol Ecol 2: 113-118.
45. White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR Protocols: A Guide to Methods and Applications. New York: Academic Press Inc. pp. 315-322.
46. Schwan RF, Rose AH, Board RG (1995) Microbial fermentation of cocoa beans, with emphasis on enzymatic degradation of the pulp. J Appl Bacteriol (Symp Suppl) 79: 96S-107S.
47. Lefeber T, Papalexandratou Z, Gobert W, Camu N, De Vuyst L (2011) Onfarm implementation of a starter culture for improved cocoa bean fermentation and its influence on the flavour of chocolates produced thereof. Food Microbiol 30: 379-392.
48. Schwan RF (1998) Cocoa fermentations conducted with a defined microbial cocktail inoculum. Appl Environ Microbiol 64: 1477-1483.