Unraveling core functional microbiota in traditional solid-state fermentation by high-throughput amplicons and metatranscriptomics sequencing

Frontiers in Microbiology

Volumn 8, Issue JUL, 2017, Pages

  Song, Zhewei ^a   Du, Hai ^a   Zhang, Yan ^b   Xu, Yan ^a  

^a JIANGNAN UNIVERSITY   (China)

^b Shanghai Jiao Tong University   (China)

Author keywords

Amplicons; Core functional microbiota; Fermentation microbiota; Functional shift; High throughput sequencing; Metatranscriptomics; Microbial succession; Solid state fermentation

Indexed keywords

ACETIC ACID; ALCOHOL; LACTIC ACID; RNA 16S;

ALCOHOL PRODUCTION; AMPLICON; ARTICLE; DNA EXTRACTION; DOWN REGULATION; GENE EXPRESSION; HIGH THROUGHPUT SEQUENCING; LACTOBACILLUS; MASS FRAGMENTOGRAPHY; MICROBIAL DIVERSITY; MICROFLORA; MOISTURE; NONHUMAN; PH; PHYLOGENY; POPULATION ABUNDANCE; SACCHAROMYCES; SEQUENCE ANALYSIS; SOLID STATE FERMENTATION; TEMPERATURE; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; UPREGULATION;

EID: 85023770063     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.01294     Document Type: Article

References (87)

1. Aldrete-Tapia, A., Escobar-Ramírez, M. C., Tamplin, M. L., and Hernández-Iturriaga, M. (2014). High-throughput sequencing of microbial communities in Poro cheese, an artisanal Mexican cheese. Food Microbiol. 44, 136-141. doi: 10.1016/j.fm.2014.05.022
2. Angly, F. E., Heath, C., Morgan, T. C., Tonin, H., Rich, V., Schaffelke, B., et al. (2016). Marine microbial communities of the Great Barrier Reef lagoon are influenced by riverine floodwaters and seasonal weather events. Peer J. 4:e1511. doi: 10.7717/peerj.1511
3. Araque, I., Bordons, A., and Reguant, C. (2013). Effect of ethanol and low pH on citrulline and ornithine excretion and arc gene expression by strains of Lactobacillus brevis and Pediococcus pentosaceus. Food Microbiol. 33, 107-113. doi: 10.1016/j.fm.2012.09.005
4. Astudillo-Garcia, C., Bell, J. J., Webster, N. S., Glasl, B., Jompa, J., Montoya, J. M., et al. (2017). Evaluating the core microbiota in complex communities: a systematic investigation. Environ. Microbiol. 19, 1450-1462. doi: 10.1111/1462-2920.13647
5. Azwar, M. Y., Hussain, M. A., and Abdul-Wahab, A. K. (2014). Development of biohydrogen production by photobiological, fermentation and electrochemical processes: a review. Renew. Sustain. Energy Rev. 31, 158-173. doi: 10.1016/j.rser.2013.11.022
6. Bokulich, N. A., and Mills, D. A. (2012). Next-generation approaches to the microbial ecology of food fermentations. BMB Rep. 45, 377-389. doi: 10.5483/BMBRep.2012.45.7.148
7. Bolger, A. M., Lohse, M., and Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114-2120. doi: 10.1093/bioinformatics/btu170
8. Borkowf, C. B. (2002). Computing the nonnull asymptotic variance and the asymptotic relative efficiency of Spearman's rank correlation. Comput. Stat. Data Anal. 39, 271-286. doi: 10.1016/S0167-9473(01)00081-0
9. Buchfink, B., Xie, C., and Huson, D. H. (2015). Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59-60. doi: 10.1038/nmeth.3176
10. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., et al. (2010). QIIME allows analysis of high-throughput microbiota sequencing data. Nat. Med. 7, 335-336. doi: 10.1038/nmeth.f.303
11. Chen, B., Wu, Q., and Xu, Y. (2014). Filamentous fungal diversity and community structure associated with the solid state fermentation of Chinese Maotai-flavor liquor. Int. J. Food Microbiol. 179, 80-84. doi: 10.1016/j.ijfoodmicro.2014.03.011
12. Chen, Y., Wen, Y., Tang, Z., Huang, J., Zhou, Q., and Vymazal, J. (2015). Effects of plant biomass on bacterial microbiota structure in constructed wetlands used for tertiary wastewater treatment. Ecol. Eng. 84, 38-45. doi: 10.1016/j.ecoleng.2015.07.013
13. Cocolin, L., Alessandria, V., Dolci, P., Gorra, R., and Rantsiou, K. (2013). Culture independent methods to assess the diversity and dynamics of microbiota during food fermentation. Int. J. Food Microbiol. 167, 29-43. doi: 10.1016/j.ijfoodmicro.2013.05.008
14. Cordovez, V., Carrion, V. J., Etalo, D. W., Mumm, R., Zhu, H., Van Wezel, G. P., et al. (2015). Diversity and functions of volatile organic compounds produced by Streptomyces from a disease-suppressive soil. Front. Microbiol. 6:1081. doi: 10.3389/fmicb.2015.01081
15. Crowley, S., Mahony, J., and van Sinderen, D. (2013). Current perspectives on antifungal lactic acid bacteria as natural bio-preservatives. Trends Food Sci. Technol. 33, 93-109. doi: 10.1016/j.tifs.2013.07.004
16. De Filippis, F., Genovese, A., Ferranti, P., Gilbert, J. A., and Ercolini, D. (2016). Metatranscriptomics reveals temperature-driven functional changes in microbiome impacting cheese maturation rate. Sci. Rep. 6:21871. doi: 10.1038/srep21871
17. Deng, W., Wang, Y., Liu, Z., Cheng, H., and Xue, Y. (2014). HemI: a toolkit for illustrating heatmaps. PLoS ONE 9:e111988. doi: 10.1371/journal.pone.0111988
18. Di Cagno, R., Pontonio, E., Buchin, S., De Angelis, M., Lattanzi, A., Valerio, F., et al. (2014). Diversity of the lactic acid bacteria and yeast microbiota switching from firm to liquid sourdough fermentation. Appl. Environ. Microbiol. 80, 3161-3172. doi: 10.1128/AEM.00309-14
19. Edirisinghe, J. N., Weisenhorn, P., Conrad, N., Xia, F., Overbeek, R., Stevens, R. L., et al. (2016). Modeling central metabolism and energy biosynthesis across microbial life. BMC Genomics 17:568. doi: 10.1186/s12864-016-2887-8
20. Ercolini, D. (2013). High-throughput sequencing and metagenomics: moving forward in the culture-independent analysis of food microbial ecology. Appl. Environ. Microbiol. 79, 3148-3155. doi: 10.1128/AEM.00928-13
21. Fierer, N., Ladau, J., Clemente, J. C., Leff, J. W., Owens, S. M., Pollard, K. S., et al. (2013). Reconstructing the microbial diversity and function of pre-agricultural tallgrass prairie soils in the United States. Science 342, 621-624. doi: 10.1126/science.1243768
22. Fröhlich-Wyder, M. T., Bisig, W., Guggisberg, D., Irmler, S., Jakob, E., and Wechsler, D. (2015). Influence of low pH on the metabolic activity of Lactobacillus buchneri and Lactobacillus parabuchneri strains in Tilsit-type model cheese. Dairy Sci. Technol. 95, 569-585. doi: 10.1007/s13594-015-0238-1
23. Gänzle, M., and Ripari, V. (2016). Composition and function of sourdough microbiota: from ecological theory to bread quality. Int. J. Food Microbiol. 239, 19-25. doi: 10.1016/j.ijfoodmicro.2016.05.004
24. Gänzle, M. G. (2015). Lactic metabolism revisited: metabolism of lactic acid bacteria in food fermentations and food spoilage. Curr. Opin. Food Sci. 2, 106-117. doi: 10.1016/j.cofs.2015.03.001
25. Garrote, G. L., Abraham, A. G., and Rumbo, M. (2015). Is lactate an undervalued functional component of fermented food products? Front. Microbiol. 6:629. doi: 10.3389/fmicb.2015.00629
26. Giraffa, G. (2004). Studying the dynamics of microbial populations during food fermentation. FEMS Microbiol. Rev. 28, 251-260. doi: 10.1016/j.femsre.2003.10.005
27. Glass, J. B., Kretz, C. B., Ganesh, S., Ranjan, P., Seston, S. L., Buck, K. N., et al. (2015). Meta-omic signatures of microbial metal and nitrogen cycling in marine oxygen minimum zones. Front. Microbiol. 6:998. doi: 10.3389/fmicb.2015.00998
28. Graham, E. B., Wieder, W. R., Leff, J. W., Weintraub, S. R., Townsend, A. R., Cleveland, C. C., et al. (2014). Do we need to understand microbial communities to predict ecosystem function? A comparison of statistical models of nitrogen cycling processes. Soil Biol. Biochem. 68, 279-282. doi: 10.1016/j.soilbio.2013.08.023
29. Gulati, A., Swarnkar, M. K., Vyas, P., Rahi, P., Thakur, R., Thakur, N., et al. (2015). Complete genome sequence of the rhizobacterium Pseudomonas trivialis strain IHBB745 with multiple plant growth-promoting activities and tolerance to desiccation and alkalinity. Genome Announc. 3:e00943-15. doi: 10.1128/genomeA.00943-15
30. Guo, Y., Li, C. I., Ye, F., and Shyr, Y. (2013). Evaluation of read count based RNAseq analysis methods. BMC Genomics 14:S2. doi: 10.1186/1471-2164-14-S8-S2
31. Haas, B. J., Papanicolaou, A., Yassour, M., Grabherr, M., Blood, P. D., Bowden, J., et al. (2013). De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8, 1494-1512. doi: 10.1038/nprot.2013.084
32. Hallin, P. F., and Ussery, D. W. (2004). CBS Genome Atlas Database: a dynamic storage for bioinformatic results and sequence data. Bioinformatics 20, 3682-3686. doi: 10.1093/bioinformatics/bth423
33. Huson, D. H., Auch, A. F., Qi, J., and Schuster, S. C. (2007). MEGAN analysis of metagenomic data. Genome Res. 17, 377-386. doi: 10.1101/gr.5969107
34. Jacomy, M., Venturini, T., Heymann, S., and Bastian, M. (2014). ForceAtlas2, a continuous graph layout algorithm for handy network visualization designed for the Gephi software. PLoS ONE 9:e98679. doi: 10.1371/journal.pone.0098679
35. Johanningsmeier, S. D., and McFeeters, R. F. (2015). Metabolic footprinting of Lactobacillus buchneri strain LA1147 during anaerobic spoilage of fermented cucumbers. Int. J. Food Microbiol. 215, 40-48. doi: 10.1016/j.ijfoodmicro.2015.08.004
36. Jung, J. Y., Lee, S. H., Jin, H. M., Hahn, Y., Madsen, E. L., and Jeon, C. O. (2013). Metatranscriptomic analysis of lactic acid bacterial gene expression during kimchi fermentation. Int. J. Food Microbiol. 163, 171-179. doi: 10.1016/j.ijfoodmicro.2013.02.022
37. Kable, M. E., Srisengfa, Y., Laird, M., Zaragoza, J., McLeod, J., Heidenreich, J., et al. (2016). The core and seasonal microbiota of raw bovine milk in tanker trucks and the impact of transfer to a milk processing facility. MBio 7:e00836-16. doi: 10.1128/mBio.00836-16
38. Kanehisa, M., Goto, S., Kawashima, S., Okuno, Y., and Hattori, M. (2004). The KEGG resource for deciphering the genome. Nucleic Acids Res. 32, D277-D280. doi: 10.1093/nar/gkh063
39. Kawahata, M., Masaki, K., Fujii, T., and Iefuji, H. (2006). Yeast genes involved in response to lactic acid and acetic acid: acidic conditions caused by the organic acids in Saccharomyces cerevisiae cultures induce expression of intracellular metal metabolism genes regulated by Aft1p. FEMS Yeast Res. 6, 924-936. doi: 10.1111/j.1567-1364.2006.00089.x
40. Kim, S. A., Lee, M. K., Park, T. H., and Rhee, M. S. (2013). A combined intervention using fermented ethanol and supercritical carbon dioxide to control Bacillus cereus and Bacillus subtilis in rice. Food Control 32, 93-98. doi: 10.1016/j.foodcont.2012.11.016
41. Kõljalg, U., Nilsson, R. H., Abarenkov, K., Tedersoo, L., Taylor, A. F., Bahram, M., et al. (2013). Towards a unified paradigm for sequence-based identification of fungi. Mol. Ecol. 22, 5271-5277. doi: 10.1111/mec.12481
42. Kong, Y., Wu, Q., Zhang, Y., and Xu, Y. (2014). In situ analysis of metabolic characteristics reveals the key yeast in the spontaneous and solid-state fermentation process of Chinese light-style liquor. Appl. Environ. Microbiol. 80, 3667-3676. doi: 10.1128/AEM.04219-13
43. Lahtinen, S., Ouwehand, A. C., Salminen, S., and von Wright, A. (eds) (2012). Lactic Acid Bacteria: Microbiological and Functional Aspects, 4th Edn. New York, NY: CRC Press
44. Lin, Z. R., Zeng, X. A., Yu, S. J., and Sun, D. W. (2012). Enhancement of ethanol-acetic acid esterification under room temperature and non-catalytic condition via pulsed electric field application. Food Bioprocess Technol. 5, 2637-2645. doi: 10.1007/s11947-011-0678-4
45. Lindahl, L., Genheden, S., Eriksson, L. A., Olsson, L., and Bettiga, M. (2016). Sphingolipids contribute to acetic acid resistance in Zygosaccharomyces bailii. Biotechnol. Bioeng. 113, 744-753. doi: 10.1002/bit.25845
46. Liu, T., Zhu, S., Tang, Q., Chen, P., Yu, Y., and Tang, S. (2013). De novo assembly and characterization of transcriptome using Illumina paired-end sequencing and identification of CesA gene in ramie (Boehmeria nivea L. Gaud). BMC Genomics 14:125. doi: 10.1186/1471-2164-14-125
47. Liu, Y., Tang, H., Lin, Z., and Xu, P. (2015). Mechanisms of acid tolerance in bacteria and prospects in biotechnology and bioremediation. Biotechnol. Adv. 33, 1484-1492. doi: 10.1016/j.biotechadv.2015.06.001
48. Long, Y., Yi, H., Chen, S., Zhang, Z., Cui, K., Bing, Y., et al. (2016a). Influences of plant type on bacterial and archaeal communities in constructed wetland treating polluted river water. Environ. Sci. Pollut. Res. Int. 23, 19570-19579. doi: 10.1007/s11356-016-7166-3
49. Long, Y., Zhang, Z., Pan, X., Li, B., Xie, S., and Guo, Q. (2016b). Substrate influences on archaeal and bacterial assemblages in constructed wetland microcosms. Ecol. Eng. 94, 437-442. doi: 10.1016/j.ecoleng.2016.06.015
50. Lu, Z. M., Liu, N., Wang, L. J., Wu, L. H., Gong, J. S., Yu, Y. J., et al. (2016). Elucidating and regulating the acetoin production role of microbial functional groups in multispecies acetic acid fermentation. Appl. Environ. Microbiol. 82, 5860-5868. doi: 10.1128/AEM.01331-16
51. McGovern, P. E., Zhang, J., Tang, J., Zhang, Z., Hall, G. R., Moreau, R. A., et al. (2004). Fermented beverages of pre-and proto-historic China. Proc. Natl. Acad. Sci. U.S.A. 101, 17593-17598. doi: 10.1073/pnas.0407921102
52. Messaoudi, S., Manai, M., Kergourlay, G., Prévost, H., Connil, N., Chobert, J. M., et al. (2013). Lactobacillus salivarius: bacteriocin and probiotic activity. Food Microbiol. 36, 296-304. doi: 10.1016/j.fm.2013.05.010
53. Papagianni, M. (2014). Recent advances in solid-state fermentation applications for the food industry. Curr. Biochem. Eng. 1, 2-8
54. Papalexandratou, Z., Lefeber, T., Bahrim, B., Lee, O. S., Daniel, H. M., and De Vuyst, L. (2013). Hanseniaspora opuntiae, Saccharomyces cerevisiae, Lactobacillus fermentum, and Acetobacter pasteurianus predominate during well-performed Malaysian cocoa bean box fermentations, underlining the importance of these microbial species for a successful cocoa bean fermentation process. Food Microbiol. 35, 73-85. doi: 10.1016/j.fm.2013.02.015
55. Pitt, J. I., and Hocking, A. D. (2009). Fungi and Food Spoilage. London: Springer
56. Qi, Z., Yang, H., Xia, X., Wang, W., and Yu, X. (2014). High strength vinegar fermentation by Acetobacter pasteurianus via enhancing alcohol respiratory chain. Biotechnol. Bioprocess Eng. 19, 289-297. doi: 10.1007/s12257-013-0727-0
57. Rantsiou, K., and Cocolin, L. (2006). New developments in the study of the microbiota of naturally fermented sausages as determined by molecular methods: a review. Int. J. Food Microbiol. 108, 255-267. doi: 10.1016/j.ijfoodmicro.2005.11.013
58. Ricciardi, A., Guidone, A., Ianniello, R. G., Cioffi, S., Aponte, M., Pavlidis, D., et al. (2015). A survey of non-starter lactic acid bacteria in traditional cheeses: culture dependent identification and survival to simulated gastrointestinal transit. Int. Dairy J. 43, 42-50. doi: 10.1016/j.idairyj.2014.11.006
59. Ryu, E. H., Yang, E. J., Woo, E. R., and Chang, H. C. (2014). Purification and characterization of antifungal compounds from Lactobacillus plantarum HD1 isolated from kimchi. Food Microbiol. 41, 19-26. doi: 10.1016/j.fm.2014.01.011
60. Schmitt, S., Tsai, P., Bell, J., Fromont, J., Ilan, M., Lindquist, N., et al. (2012). Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J. 6, 564-576. doi: 10.1038/ismej.2011.116
61. Schoch, C. L., Seifert, K. A., Huhndorf, S., Robert, V., Spouge, J. L., Levesque, C. A., et al. (2012). Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc. Natl. Acad. Sci. U.S.A 109, 6241-6246. doi: 10.1073/pnas.1117018109
62. Sekwati-Monang, B., Valcheva, R., and Gänzle, M. G. (2012). Microbial ecology of sorghum sourdoughs: effect of substrate supply and phenolic compounds on composition of fermentation microbiota. Int. J. Food Microbiol. 159, 240-246. doi: 10.1016/j.ijfoodmicro.2012.09.013
63. Solieri, L., Dakal, T. C., and Giudici, P. (2013). Next-generation sequencing and its potential impact on food microbial genomics. Ann. Microbiol. 63, 21-37. doi: 10.1007/s13213-012-0478-8
64. Sowards, J. W., Williamson, C. H. D., Weeks, T. S., McColskey, J. D., and Spear, J. R. (2014). The effect of Acetobacter sp. and a sulfate-reducing bacterial consortium from ethanol fuel environments on fatigue crack propagation in pipeline and storage tank steels. Corros. Sci. 79, 128-138. doi: 10.1016/j.corsci.2013.10.036
65. Stegen, J. C., Hurlbert, A. H., Bond-Lamberty, B., Chen, X., Anderson, C. G., Chu, R. K., et al. (2016). Aligning the measurement of microbial diversity with macroecological theory. Front. Microbiol. 7:1487. doi: 10.3389/fmicb.2016.01487
66. Su, J., Wang, T., Wang, Y., Li, Y. Y., and Li, H. (2014). The use of lactic acid-producing, malic acid-producing, or malic acid-degrading yeast strains for acidity adjustment in the wine industry. Appl. Microbiol. Biotechnol. 98, 2395-2413. doi: 10.1007/s00253-014-5508-y
67. Sulaiman, J., Gan, H. M., Yin, W. F., and Chan, K. G. (2014). Microbial succession and the functional potential during the fermentation of Chinese soy sauce brine. Front. Microbiol. 5:556. doi: 10.3389/fmicb.2014.00556
68. Tamang, J. P., Shin, D. H., Jung, S. J., and Chae, S. W. (2016). Functional properties of microorganisms in fermented foods. Front. Microbiol. 7:578. doi: 10.3389/fmicb.2016.00578
69. Tamarit, D., Ellegaard, K. M., Wikander, J., Olofsson, T., Vásquez, A., and Andersson, S. G. (2015). Functionally structured genomes in Lactobacillus kunkeei colonizing the honey crop and food products of honeybees and stingless bees. Genome Biol. Evol. 7, 1455-1473. doi: 10.1093/gbe/evv079
70. Tao, Y., Li, J., Rui, J., Xu, Z., Zhou, Y., Hu, X., et al. (2014). Prokaryotic communities in pit mud from different-aged cellars used for the production of Chinese strong-flavored liquor. Appl. Environ. Microbiol. 80, 2254-2260. doi: 10.1128/AEM.04070-13
71. Thomas, L., Larroche, C., and Pandey, A. (2013). Current developments in solid-state fermentation. Biochem. Eng. J. 81, 146-161. doi: 10.1016/j.bej.2013.10.013
72. Wang, S. Y., Ho, Y. F., Chen, Y. P., and Chen, M. J. (2015). Effects of a novel encapsulating technique on the temperature tolerance and anti-colitis activity of the probiotic bacterium Lactobacillus kefiranofaciens M1. Food Microbiol. 46, 494-500. doi: 10.1016/j.fm.2014.09.015
73. Wang, X., Fan, W., and Xu, Y. (2014). Comparison on aroma compounds in Chinese soy sauce and strong aroma type liquors by gas chromatography-olfactometry, chemical quantitative and odor activity values analysis. Eur. Food Res. Technol. 239, 813-825. doi: 10.1007/s00217-014-2275-z
74. Wang, Z., Zhang, X. X., Lu, X., Liu, B., Li, Y., Long, C., et al. (2014). Abundance and diversity of bacterial nitrifiers and denitrifiers and their functional genes in tannery wastewater treatment plants revealed by high-throughput sequencing. PLoS ONE 9:e113603. doi: 10.1371/journal.pone.0113603
75. Wang, Z. M., Lu, Z. M., Shi, J. S., and Xu, Z. H. (2016). Exploring flavour-producing core microbiota in multispecies solid-state fermentation of traditional Chinese vinegar. Sci. Rep. 6:26818. doi: 10.1038/srep26818
76. Whiteson, K. L., Lazarevic, V., Tangomo-Bento, M., Girard, M., Maughan, H., Pittet, D., et al. (2014). Noma affected children from Niger have distinct oral microbial communities based on high-throughput sequencing of 16S rRNA gene fragments. PLoS Negl. Trop. Dis. 8:e3240. doi: 10.1371/journal.pntd.0003240
77. Wolfe, B. E., Button, J. E., Santarelli, M., and Dutton, R. J. (2014). Cheese rind communities provide tractable systems for in situ and in vitro studies of microbial diversity. Cell 158, 422-433. doi: 10.1016/j.cell.2014.05.041
78. Wu, Q., Chen, L., and Xu, Y. (2013). Yeast community associated with the solid state fermentation of traditional Chinese Maotai-flavor liquor. Int. J. Food Microbiol. 166, 323-330. doi: 10.1016/j.ijfoodmicro.2013.07.003
79. Wu, Q., Xu, Y., and Chen, L. (2012). Diversity of yeast species during fermentative process contributing to Chinese Maotai-flavour liquor making. Lett. Appl. Microbiol. 55, 301-307. doi: 10.1111/j.1472-765X.2012.03294.x
80. Xu, Y., and Ji, K. (2012). "Moutai (Maotai): production and sensory properties, " in The Alcoholic Beverages: Sensory Evaluation and Consumer Research, ed. J. Piggott (Sawston: Woodhead Publishing), 315-330
81. Xu, Y., Wang, D., Fan, W. L., Mu, X. Q., and Chen, J. (2010). Traditional Chinese biotechnology. Adv. Biochem. Eng. Biotechnol. 122, 189-233. doi: 10.1007/10_2008_36
82. Yuangsaard, N., Yongmanitchai, W., Yamada, M., and Limtong, S. (2013). Selection and characterization of a newly isolated thermotolerant Pichia kudriavzevii strain for ethanol production at high temperature from cassava starch hydrolysate. Antonie Van Leeuwenhoek 103, 577-588. doi: 10.1007/s10482-012-9842-8
83. Zhang, J., Guo, Z., Xue, Z., Sun, Z., Zhang, M., Wang, L., et al. (2015). A phylo-functional core of gut microbiota in healthy young Chinese cohorts across lifestyles, geography and ethnicities. ISME J. 9, 1979-1990. doi: 10.1038/ismej.2015.11
84. Zhu, S., Lu, X., Ji, K., Guo, K., Li, Y., Wu, C., et al. (2007). Characterization of flavor compounds in Chinese liquor Moutai by comprehensive two-dimensional gas chromatography/time-of-flight mass spectrometry. Anal. Chim. Acta 597, 340-348. doi: 10.1128/AEM.00594-15
85. Zhu, X., Siegert, M., Yates, M. D., and Logan, B. E. (2015). Alamethicin suppresses methanogenesis and promotes acetogenesis in bioelectrochemical systems. Appl. Environ. Microbiol. 81, 3863-3868. doi: 10.1016/j.aca.2007.07.007
86. Ziesemer, K. A., Mann, A. E., Sankaranarayanan, K., Schroeder, H., Ozga, A. T., Brandt, B. W., et al. (2015). Intrinsic challenges in ancient microbiome reconstruction using 16S rRNA gene amplification. Sci. Rep. 5:16498. doi: 10.1038/srep16498
87. Zothanpuia, A. K. P., Chandra, P., Leo, V. V., Mishra, V. K., Kumar, B., and Singh, B. P. (2017). Production of potent antimicrobial compounds from Streptomyces cyaneofuscatus associated with fresh water sediment. Front. Microbiol. 8:68. doi: 10.3389/fmicb.2017.00068