Carrot juice fermentations as man-made microbial ecosystems dominated by lactic acid bacteria

Applied and Environmental Microbiology

Volumn 84, Issue 12, 2018, Pages

  Wuyts, Sander ^a,b   Van Beeck, Wannes ^a   Oerlemans, Eline F M ^a   Wittouck, Stijn ^a   Claes, Ingmar J J ^a   De Boeck, Ilke ^a   Weckx, Stefan ^b   Lievens, Bart ^c   De Vuyst, Luc ^b   Lebeer, Sarah ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^c UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

16S RNA sequencing; Amplicon; RNA based 16S amplicon sequencing

Indexed keywords

AMINES; BACTERIA; ECOSYSTEMS; GENE ENCODING; LABORATORIES; LACTIC ACID; NUCLEIC ACIDS; RNA;

16S RRNA GENE SEQUENCING; AMPLICONS; FERMENTATION DYNAMICS; LACTIC ACID BACTERIA; MICROBIAL ECO SYSTEM; PHYLOGENETIC GROUPS; RNA SEQUENCING; SPONTANEOUS FERMENTATION;

FERMENTATION;

BACTERIUM; CHEMICAL COMPOUND; FERMENTATION; MICROBIAL ACTIVITY; MICROBIAL ECOLOGY; MICROBIOLOGY; PLANT PRODUCT; RELATIVE ABUNDANCE; RNA;

BACTERIA (MICROORGANISMS); DAUCUS CAROTA; ENTEROBACTERIACEAE; LACTOBACILLUS; LEUCONOSTOC;

RNA 16S;

ANTIBIOSIS; BACTERIAL COUNT; BIODIVERSITY; CARROT; CLASSIFICATION; ENTEROBACTERIACEAE; FERMENTATION; FOOD CONTROL; FRUIT AND VEGETABLE JUICE; GENETICS; ISOLATION AND PURIFICATION; LACTOBACILLALES; LEUCONOSTOC; MICROBIOLOGY; PHYLOGENY;

ANTIBIOSIS; BIODIVERSITY; COLONY COUNT, MICROBIAL; DAUCUS CAROTA; ENTEROBACTERIACEAE; FERMENTATION; FOOD MICROBIOLOGY; FRUIT AND VEGETABLE JUICES; LACTOBACILLALES; LEUCONOSTOC; PHYLOGENY; RNA, RIBOSOMAL, 16S;

EID: 85047839090     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00134-18     Document Type: Article

References (70)

1. Leroy F, De Vuyst L. 2014. Fermented food in the context of a healthy diet. Curr Opin Clin Nutr Metab Care 17:574-581. https://doi.org/10 .1097/MCO.0000000000000108
2. Hayden B, Canuel N, Shanse J. 2013. What was brewing in the Natufian? An archaeological assessment of brewing technology in the Epipaleolithic. J Archaeol Method Theory 20:102-150. https://doi.org/10.1007/ s10816-011-9127-y
3. Di Cagno R, Coda R, De Angelis M, Gobbetti M. 2013. Exploitation of vegetables and fruits through lactic acid fermentation. Food Microbiol 33:1-10. https://doi.org/10.1016/j.fm.2012.09.003
4. Marco ML, Heeney D, Binda S, Cifelli CJ, Cotter PD, Foligné B, Gänzle M, Kort R, Pasin G, Pihlanto A, Smid EJ, Hutkins R. 2017. Health benefits of fermented foods: microbiota and beyond. Curr Opin Biotechnol 44: 94-102. https://doi.org/10.1016/j.copbio.2016.11.010
5. Marsh AJ, Hill C, Ross RP, Cotter PD. 2014. Fermented beverages with health-promoting potential: past and future perspectives. Trends Food Sci Technol 38:113-124. https://doi.org/10.1016/j.tifs.2014.05.002
6. Filannino P, Cardinali G, Rizzello CG, Buchin S, De Angelis M, Gobbetti M, Di Cagno R. 2014. Metabolic responses of Lactobacillus plantarum strains during fermentation and storage of vegetable and fruit juices. Appl Environ Microbiol 80:2206-2215. https://doi.org/10.1128/AEM.03885-13
7. Rivera-Espinoza Y, Gallardo-Navarro Y. 2010. Non-dairy probiotic products. Food Microbiol 27:1-11. https://doi.org/10.1016/j.fm.2008.06.008
8. Lebeer S, Vanderleyden J, De Keersmaecker SCJ. 2008. Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev 72:728-764. https://doi.org/10.1128/MMBR.00017-08
9. Sanders ME, Benson A, Lebeer S, Merenstein DJ, Klaenhammer TR. 2018. Shared mechanisms among probiotic taxa: implications for general probiotic claims. Curr Opin Biotechnol 49:207-216. https://doi.org/10 .1016/j.copbio.2017.09.007
10. Lebeer S, Bron PA, Marco ML, Motherway MOC, Hill C, Pot B, Roos S, Klaenhammer T. 2018. Identification of probiotic effector molecules: present state and future perspectives. Curr Opin Biotechnol 49:217-223. https://doi.org/10.1016/j.copbio.2017.10.007
11. Cocolin L, Gobbetti M, Neviani E, Daffonchio D. 2016. Ensuring safety in artisanal food microbiology. Nat Microbiol 1:16171. https://doi.org/10 .1038/nmicrobiol.2016.171
12. De Filippis F, Genovese A, Ferranti P, Gilbert JA, Ercolini D. 2016. Metatranscriptomics reveals temperature-driven functional changes in microbiome impacting cheese maturation rate. Sci Rep 6:21871. https://doi .org/10.1038/srep21871
13. Leroy F, De Vuyst L. 2004. Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci Technol 15:67-78. https://doi.org/10.1016/j.tifs.2003.09.004
14. Di Cagno R, Surico RF, Siragusa S, De Angelis M, Paradiso A, Minervini F, De Gara L, Gobbetti M. 2008. Selection and use of autochthonous mixed starter for lactic acid fermentation of carrots, French beans or marrows. Int J Food Microbiol 127:220-228. https://doi.org/10.1016/j.ijfoodmicro .2008.07.010
15. Di Cagno R, Surico RF, Paradiso A, De Angelis M, Salmon JC, Buchin S, De Gara L, Gobbetti M. 2009. Effect of autochthonous lactic acid bacteria starters on health-promoting and sensory properties of tomato juices. Int J Food Microbiol 128:473-483. https://doi.org/10.1016/j.ijfoodmicro .2008.10.017
16. Wouters D, Grosu-Tudor S, Zamfir M, De Vuyst L. 2013. Bacterial community dynamics, lactic acid bacteria species diversity and metabolite kinetics of traditional Romanian vegetable fermentations. J Sci Food Agric 93:749-760. https://doi.org/10.1002/jsfa.5788
17. Bernaert N, Wouters D, De Vuyst L, De Paepe D, De Clercq H, Van Bockstaele E, De Loose M, Van Droogenbroeck B. 2013. Antioxidant changes of leek (Allium ampeloprasum var. porrum) during spontaneous fermentation of the white shaft and green leaves. J Sci Food Agric 93:2146-2153. https://doi.org/10.1002/jsfa.6020
18. Nazzaro F, Fratianni F, Sada A, Orlando P. 2008. Synbiotic potential of carrot juice supplemented with Lactobacillus spp. and inulin or fructooligosaccharides. J Sci Food Agric 88:2271-2276. https://doi.org/10.1002/ jsfa.3343
19. Filannino P, Di Cagno R, Crecchio C, De Virgilio C, De Angelis M, Gobbetti M. 2016. Transcriptional reprogramming and phenotypic switching associated with the adaptation of Lactobacillus plantarum C2 to plant niches. Sci Rep 6:27392. https://doi.org/10.1038/srep27392
20. Demir N, Bahceci KS, Acar J. 2006. The effects of different initial Lactobacillus plantarum concentrations on some properties of fermented carrot juice. J Food Process Preserv 30:352-363. https://doi.org/10.1111/ j.1745-4549.2006.00070.x
21. Gardner NJ, Savard T, Obermeier P, Caldwell G, Champagne CP. 2001. Selection and characterization of mixed starter cultures for lactic acid fermentation of carrot, cabbage, beet and onion vegetable mixtures. Int J Food Microbiol 64:261-275. https://doi.org/10.1016/S0168-1605 (00)00461-X
22. Code of Federal Regulations. 2017. Title 21. Food and drugs. Chapter I. Food and Drug Administration, Department of Health and Human Services. Subchapter B. Food for Human Consumption. Part 114. Acidified foods. 21 CFR 114.3. https://www.accessdata.fda.gov/scripts/cdrh/ cfdocs/cfcfr/CFRSearch.cfm?fr=114.3
23. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. 2016. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581-583. https://doi.org/10.1038/nmeth.3869
24. Callahan BJ, McMurdie PJ, Holmes SP. 2017. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J 11:2639-2643. https://doi.org/10.1038/ismej.2017.119
25. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J. 2017. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67: 1613-1617. https://doi.org/10.1099/ijsem.0.001755
26. Pedersen TB, Kot WP, Hansen LH, Sørensen SJ, Broadbent JR, Vogensen FK, Ardö Y. 2014. Genome sequences of two Leuconostoc pseudomesenteroides strains isolated from Danish dairy starter cultures. Genome Announc 2:e00484-14. https://doi.org/10.1128/genomeA.00484-14
27. Duar RM, Lin XB, Zheng J, Martino ME, Grenier T, Pérez-Muñoz ME, Leulier F, Gänzle M, Walter J. 2017. Lifestyles in transition: evolution and natural history of the genus Lactobacillus. FEMS Microbiol Rev 41: S27-S48. https://doi.org/10.1093/femsre/fux030
28. Zheng J, Ruan L, Sun M, Gänzle M. 2015. A genomic view of lactobacilli and pediococci demonstrates that phylogeny matches ecology and physiology. Appl Environ Microbiol 81:7233-7243. https://doi.org/10 .1128/AEM.02116-15
29. Wuyts S, Wittouck S, De Boeck I, Allonsius CN, Pasolli E, Segata N, Lebeer S. 2017. Large-scale phylogenomics of the Lactobacillus casei group highlights taxonomic inconsistencies and reveals novel cladeassociated features. mSystems 2:e00061-17. https://doi.org/10.1128/ mSystems.00061-17
30. Wolfe BE, Dutton RJ. 2015. Fermented foods as experimentally tractable microbial ecosystems. Cell 161:49-55. https://doi.org/10.1016/j.cell.2015 .02.034
31. Pérez-Díaz IM, Hayes J, Medina E, Anekella K, Daughtry K, Dieck S, Levi M, Price R, Butz N, Lu Z, Azcarate-Peril MA. 2016. Reassessment of the succession of lactic acid bacteria in commercial cucumber fermentations and physiological and genomic features associated with their dominance. Food Microbiol 63:217-227
32. Park E-J, Chun J, Cha C-J, Park W-S, Jeon CO, Bae J-W. 2012. Bacterial community analysis during fermentation of ten representative kinds of kimchi with barcoded pyrosequencing. Food Microbiol 30:197-204. https://doi.org/10.1016/j.fm.2011.10.011
33. Wouters D, Bernaert N, Anno N, Van Droogenbroeck B, De Loose M, Van Bockstaele E, De Vuyst L. 2013. Application and validation of autochthonous lactic acid bacteria starter cultures for controlled leek fermentations and their influence on the antioxidant properties of leek. Int J Food Microbiol 165:121-133. https://doi.org/10.1016/j .ijfoodmicro.2013.04.016
34. Leff JW, Fierer N. 2013. Bacterial communities associated with the surfaces of fresh fruits and vegetables. PLoS One 8:e59310. https://doi.org/ 10.1371/journal.pone.0059310
35. Abadias M, Usall J, Anguera M, Solsona C, Viñas I. 2008. Microbiological quality of fresh, minimally-processed fruit and vegetables, and sprouts from retail establishments. Int J Food Microbiol 123:121-129. https://doi .org/10.1016/j.ijfoodmicro.2007.12.013
36. Rastogi G, Sbodio A, Tech JJ, Suslow TV, Coaker GL, Leveau JHJ. 2012. Leaf microbiota in an agroecosystem: spatiotemporal variation in bacterial community composition on field-grown lettuce. ISME J 6:1812-1822. https://doi.org/10.1038/ismej.2012.32
37. Berg G, Erlacher A, Smalla K, Krause R. 2014. Vegetable microbiomes: is there a connection among opportunistic infections, human health and our "gut feeling"? Microb Biotechnol 7:487-495. https://doi.org/10.1111/ 1751-7915.12159
38. Jung JY, Lee SH, Kim JM, Park MS, Bae J-W, Hahn Y, Madsen EL, Jeon CO. 2011. Metagenomic analysis of kimchi, a traditional Korean fermented food. Appl Environ Microbiol 77:2264-2274. https://doi.org/10.1128/ AEM.02157-10
39. Plengvidhya V, Breidt F, Lu Z, Fleming HP. 2007. DNA fingerprinting of lactic acid bacteria in sauerkraut fermentations. Appl Environ Microbiol 73:7697-7702. https://doi.org/10.1128/AEM.01342-07
40. De Bruyn F, Zhang SJ, Pothakos V, Torres J, Lambot C, Moroni AV, Callanan M, Sybesma W, Weckx S, De Vuyst L. 2017. Exploring the impacts of postharvest processing on the microbiota and metabolite profiles during green coffee bean production. Appl Environ Microbiol 83:e02398-16
41. Nielsen KM, Johnsen PJ, Bensasson D, Daffonchio D. 2007. Release and persistence of extracellular DNA in the environment. Environ Biosafety Res 6:37-53. https://doi.org/10.1051/ebr:2007031
42. Alessandria V, Ferrocino I, De Filippis F, Fontana M, Rantsiou K, Ercolini D, Cocolin L. 2016. Microbiota of an Italian Grana-like cheese during manufacture and ripening, unraveled by 16S rRNA-based approaches. Appl Environ Microbiol 82:3988-3995. https://doi.org/10.1128/AEM .00999-16
43. Emerson JB, Adams RI, Román CMB, Brooks B, Coil DA, Dahlhausen K, Ganz HH, Hartmann EM, Hsu T, Justice NB, Paulino-Lima IG, Luongo JC, Lymperopoulou DS, Gomez-Silvan C, Rothschild-Mancinelli B, Balk M, Huttenhower C, Nocker A, Vaishampayan P, Rothschild LJ. 2017. Schrödinger's microbes: tools for distinguishing the living from the dead in microbial ecosystems. Microbiome 5:86. https://doi.org/10.1186/ s40168-017-0285-3
44. Alvarez MA, Moreno-Arribas MV. 2014. The problem of biogenic amines in fermented foods and the use of potential biogenic amine-degrading microorganisms as a solution. Trends Food Sci Technol 39:146-155. https://doi.org/10.1016/j.tifs.2014.07.007
45. Linares DM, Del Rio B, Redruello B, Ladero V, Martin MC, Fernandez M, Ruas-Madiedo P, Alvarez MA. 2016. Comparative analysis of the in vitro cytotoxicity of the dietary biogenic amines tyramine and histamine. Food Chem 197:658-663. https://doi.org/10.1016/j.foodchem.2015.11 .013
46. McCabe-Sellers BJ, Staggs CG, Bogle ML. 2006. Tyramine in foods and monoamine oxidase inhibitor drugs: a crossroad where medicine, nutrition, pharmacy, and food industry converge. J Food Compos Anal 19:58-65
47. Gänzle MG. 2015. Lactic metabolism revisited: metabolism of lactic acid bacteria in food fermentations and food spoilage. Curr Opin Food Sci 2:106-117. https://doi.org/10.1016/j.cofs.2015.03.001
48. Kuley E, Balikci E, özoğul I, Gökdogan S, özoğul F. 2012. Stimulation of cadaverine production by foodborne pathogens in the presence of Lactobacillus, Lactococcus, and Streptococcus spp. J Food Sci 77: M650-M658. https://doi.org/10.1111/j.1750-3841.2012.02825.x
49. Pessione E, Cirrincione S. 2016. Bioactive molecules released in food by lactic acid bacteria: encrypted peptides and biogenic amines. Front Microbiol 7:876. https://doi.org/10.3389/fmicb.2016.00876
50. Spano G, Russo P, Lonvaud-Funel A, Lucas P, Alexandre H, Grandvalet C, Coton E, Coton M, Barnavon L, Bach B, Rattray F, Bunte A, Magni C, Ladero V, Alvarez M, Fernández M, Lopez P, de Palencia PF, Corbi A, Trip H, Lolkema JS. 2010. Biogenic amines in fermented foods. Eur J Clin Nutr 64:S95-S100. https://doi.org/10.1038/ejcn.2010.218
51. Wüthrich D, Berthoud H, Wechsler D, Eugster E, Irmler S, Bruggmann R. 2017. The histidine decarboxylase gene cluster of Lactobacillus parabuchneri was gained by horizontal gene transfer and is mobile within the species. Front Microbiol 8:218. https://doi.org/10.3389/ fmicb.2017.00218
52. Collins JD, Noerrung B, Budka H, Andreoletti O, Buncic S, Griffin J, Hald T, Havelaar A, Hope J, Klein G, Koutsoumanis K, McLauchlin J, Müller-Graf C, Nguyen-The C, Peixe L, Prieto Maradona M, Ricci A, Sofos J, Threlfall J, Vågsholm I, Vanopdenbosch E. 2011. Scientific opinion on risk based control of biogenic amine formation in fermented foods. EFSA J 9:2393. https://doi.org/10.2903/j.efsa.2011.2393
53. Romano A, Ladero V, Alvarez MA, Lucas PM. 2014. Putrescine production via the ornithine decarboxylation pathway improves the acid stress survival of Lactobacillus brevis and is part of a horizontally transferred acid resistance locus. Int J Food Microbiol 175:14-19. https://doi.org/10 .1016/j.ijfoodmicro.2014.01.009
54. Ladero V, Cruz Martin M, Redruello B, Mayo B, Florez AB, Fernandez M, Alvarez MA. 2015. Genetic and functional analysis of biogenic amine production capacity among starter and non-starter lactic acid bacteria isolated from artisanal cheeses. Eur Food Res Technol 241:377-383. https://doi.org/10.1007/s00217-015-2469-z
55. Sun Z, Harris HMB, McCann A, Guo C, Argimón S, Zhang W, Yang X, Jeffery IB, Cooney JC, Kagawa TF, Liu W, Song Y, Salvetti E, Wrobel A, Rasinkangas P, Parkhill J, Rea MC, O'Sullivan O, Ritari J, Douillard FP, Paul Ross R, Yang R, Briner AE, Felis GE, de Vos WM, Barrangou R, Klaenhammer TR, Caufield PW, Cui Y, Zhang H, O'Toole PW. 2015. Expanding the biotechnology potential of lactobacilli through comparative genomics of 213 strains and associated genera. Nat Commun 6:8322. https://doi .org/10.1038/ncomms9322
56. Wouters D, Grosu-Tudor S, Zamfir M, De Vuyst L. 2013. Applicability of Lactobacillus plantarum IMDO 788 as a starter culture to control vegetable fermentations. J Sci Food Agric 93:3352-3361. https://doi.org/10 .1002/jsfa.6184
57. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. 2013. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112-5120. https://doi.org/10.1128/ AEM.01043-13
58. R Core Development Team. 2006. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
59. Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM. 2014. Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42:D633-D642. https://doi.org/10.1093/nar/gkt1244
60. McMurdie PJ, Holmes S. 2013. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217. https://doi.org/10.1371/journal.pone.0061217
61. Oksanen J, Guillaume Blanchet F, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H. 2012. vegan: community ecology package. R package. R Foundation for Statistical Computing, Vienna, Austria
62. Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312-1313. https://doi.org/10.1093/bioinformatics/btu033
63. Yu G, Smith DK, Zhu H, Guan Y, Lam TTY. 2016. ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol 8:28-36. https://doi.org/ 10.1111/2041-210X.12628
64. Reference deleted
65. Lane DJ. 1991. 16S/23S rRNA sequencing, p 115-175, In Stackebrandt E, Goodfellow M (ed), Nucleic acid techniques in bacterial systematic. John Wiley & Sons, New York, NY
66. Turner S, Pryer KM, Miao VP, Palmer JD. 1999. Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 46:327-338. https:// doi.org/10.1111/j.1550-7408.1999.tb04612.x
67. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647-1649. https://doi.org/10.1093/bioinformatics/ bts199
68. Vrancken G, Rimaux T, De Vuyst L, Leroy F. 2008. Kinetic analysis of growth and sugar consumption by Lactobacillus fermentum IMDO 130101 reveals adaptation to the acidic sourdough ecosystem. Int J Food Microbiol 128:58-66. https://doi.org/10.1016/j.ijfoodmicro .2008.08.001
69. Stavropoulou DA, Borremans W, De Vuyst L, De Smet S, Leroy F. 2015. Amino acid conversions by coagulase-negative staphylococci in a rich medium: assessment of inter-and intraspecies heterogeneity. Int J Food Microbiol 212:34-40. https://doi.org/10.1016/j.ijfoodmicro.2015.04.048
70. Yamada KD, Tomii K, Katoh K. 2016. Application of the MAFFT sequence alignment program to large data-reexamination of the usefulness of chained guide trees. Bioinformatics 32:3246-3251. https://doi.org/10 .1093/bioinformatics/btw412