Abstract
Zaopocu (ZPC) is a traditional fermented food from Hainan Island with tropical characteristics, and its specific fungal community may provide its distinctive acidity, taste, and flavor. Our research investigated the profiles and diversity of the fungal composition in three types of ZPC (ZPC_A, ZPC_B, and ZPC_C) using high-throughput sequencing. The results showed that the two main phyla in all samples were Ascomycota and Basidiomycota. Significant differences existed among the various samples at the genus and species levels. The primary genus in ZPC_A samples was Candida, while Kodamaea and Saccharomyces dominated ZPC_B and ZPC_C samples, respectively. Candida sorbosivorans predominated in ZPC_A, while both ZPC_B and ZPC_C samples had Kodamaea ohmeri as the dominant species. The physicochemical properties significantly impacted the composition of the ZPC fungal communities. Titratable acidity (TA) had the most pronounced impact, whereas salinity had a negligible effect. Furthermore, the correlation between physicochemical properties and representative fungal taxa showed that three core genera, Issatchenkia, Torulaspora, and Wickerhamomyces, were positively correlated with TA. The fungal communities of the three types ZPCs were primarily dominated by pathotrophs, with the guild mode of the animal pathogen having the highest content in each sample. Moreover, some species can cause food spoilage and potentially infect humans, such as Kodamaea ohmeri and Aspergillus flavus, were identified, indicating the presence of potentially pathogenic fungal contamination during the production and distribution of ZPC. Therefore, quality control should be improved. This is the first study to provide a detailed insight into the relationship between the fungal communities and physicochemical indices of traditional fermented food from the Hainan tropical region. Our findings may aid in improving the quality and safety of ZPC.
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Data availability
The datasets analyzed during the current study are available from the corresponding author upon reasonable request.
Abbreviations
- ZPC:
-
Zaopocu
- TA:
-
Titratable Acidity
- LA:
-
Lactic Acid
- AA:
-
Amino Acid
- OTU:
-
Operational Taxonomic Units
- QIIME:
-
Quantitative Insights Into Microbial Ecology
- ITS:
-
Internal Transcribed Spacer
- LEfSe:
-
Linear Discriminant Analysis Effect Size analysis
- LDA:
-
Linear Discriminant Analysis
- PCA:
-
Principal Component Analysis
- NaOH:
-
Sodium Hydroxide
- CCA:
-
Canonical Correlation Analysis
- PCR:
-
Polymerase Chain Reaction
- UPGMA:
-
Unweighted Pair-group Method with Arithmetic means
References
Adekoya I, Obadina A, Phoku J, De Boevre M, De Saeger S, Njobeh P (2018) Fungal and mycotoxin contamination of fermented foods from selected south african markets. Food Control 90:295–303. https://doi.org/10.1016/j.foodcont.2018.02.040
Anal AK, Perpetuini G, Petchkongkaew A, Tan R, Avallone S, Tofalo R, Nguyen HV, Chu-Ky S, Ho PH, Phan TT, Wachéet Y (2020) Food safety risks in traditional fermented food from South-East Asia. Food Control 109:106922. https://doi.org/10.1016/j.foodcont.2019.106922
Bezerra-Bussoli C, Baffi MA, Gomes E, Roberto DS (2013) Yeast diversity isolated from grape musts during spontaneous fermentation from a brazilian winery. Curr Microbiol 67(3):356–361. https://doi.org/10.1007/s00284-013-0375-9
Borelli BM, Ferreira EG, Lacerda IC, Franco GR, Rosa CA (2006) Yeast populations associated with the artisanal cheese produced in the region of Serra da Canastra, Brazil. World J Microbiol Biotechnol 22:1115–1119. https://doi.org/10.1007/s11274-006-9151-3
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Casal M, Leão C (1995) Utilization of short-chain monocarboxylic acids by the yeast Torulaspora delbrueckii: specificity of the transport systems and their regulation. Biochim Biophys Acta (BBA)-Mol Cell Res 1267:122–130. https://doi.org/10.1016/0167-4889(95)00067-3
Chen S, Zhou Y, Chen Y, Gu J (2018) Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:884–890. https://doi.org/10.1093/bioinformatics/bty560
Degrain A, Manhivi V, Remize F, Garcia C, Sivakumar D (2020) Effect of lactic acid fermentation on color, phenolic compounds and antioxidant activity in african nightshade. Microorganisms 8:1324. https://doi.org/10.3390/microorganisms8091324
Du Plessis H, Du Toit M, Nieuwoudt H, Van der Rijst M, Kidd M, Jolly N (2017) Effect of Saccharomyces, non-saccharomyces yeasts and malolactic fermentation strategies on fermentation kinetics and flavor of Shiraz wines. Fermentation 3:64. https://doi.org/10.3390/fermentation3040064
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/nmeth.2604
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381
Guan Q, Zheng W, Huang T, Xiao Y, Liu Z, Peng Z, Xiong T (2020) Comparison of microbial communities and physiochemical characteristics of two traditionally fermented vegetables. Food Res Int 128:108755. https://doi.org/10.1016/j.foodres.2019.108755
Hittinger CT, Steele JL, Ryder DS (2018) Diverse yeasts for diverse fermented beverages and foods. Curr Opin Biotechnol 49:199–206. https://doi.org/10.1016/j.copbio.2017.10.004
Hu N, Lei M, Zhao X, Wang Y, Zhang Y, Wang S (2020) Analysis of microbiota in Hainan Yucha during fermentation by 16S rRNA gene high-throughput sequencing. J Food Process Preserv 44:14523. https://doi.org/10.1111/jfpp.14523
Ioannou P, Papakitsou I (2020) Kodamaea ohmeri infections in humans: a systematic review. Mycoses 63:636–643. https://doi.org/10.1111/myc.13094
Jiang S, Ma C, Peng Q, Huo D, Li W, Zhang J (2019) Microbial profile and genetic polymorphism of predominant species in some traditional fermented seafoods of the Hainan area in China. Front Microbiol 10:564. https://doi.org/10.3389/fmicb.2019.00564
Kim SS, Kwak HS, Kim MJ (2020) The effect of various salinity levels on metabolomic profiles, antioxidant capacities and sensory attributes of doenjang, a fermented soybean paste. Food Chem 328:127176. https://doi.org/10.1016/j.foodchem.2020.127176
Koo H, Andes DR, Krysan DJ (2018) Candida–streptococcal interactions in biofilm-associated oral diseases. PLoS Pathog 14(12):1007342. https://doi.org/10.1371/journal.ppat.1007342
Krishnan S, Manavathu EK, Chandrasekar PH (2009) Aspergillus flavus: an emerging non-fumigatus aspergillus species of significance. Mycoses 52:206–222. https://doi.org/10.1111/j.1439-0507.2008.01642.x
Lee MA, Choi YJ, Lee H, Hwang S, Lee HJ, Park SJ, Seo HY (2021) Influence of salinity on the microbial community composition and metabolite profile in Kimchi. Fermentation 7(4):308–321. https://doi.org/10.3390/fermentation7040308
Li D, Duan F, Tian Q, Zhong D, Wang X, Jia L (2021) Physiochemical, microbiological and flavor characteristics of traditional chinese fermented food Kaili Red Sour Soup. LWT 142:110933. https://doi.org/10.1016/j.lwt.2021.110933
Lin LJ, Du FM, Zeng J, Liang ZJ, Zhang XY, Gao XY (2020) Deep insights into fungal diversity in traditional chinese sour soup by Illumina MiSeq sequencing. Food Res Int 137:109439. https://doi.org/10.1016/j.foodres.2020.109439
Liu S, Han Y, Zhou Z (2011) Lactic acid bacteria in traditional fermented chinese foods. Food Res Int 44:643–651. https://doi.org/10.1016/j.foodres.2010.12.034
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Mendoza-Reyes DF, Gómez-Gaviria M, Mora-Montes HM (2022) Candida lusitaniae: Biology, pathogenicity, virulence factors, diagnosis, and treatment. Infect Drug Resist 15:5121–5135. https://doi.org/10.2147/IDR.S383785
Nahidul-Islam SM, Kuda T, Takahashi H, Kimura B (2018) Bacterial and fungal microbiota in traditional bangladeshi fermented milk products analysed by culture-dependent and culture-independent methods. Food Res Int 111:431–437. https://doi.org/10.1016/j.foodres.2018.05.048
Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Kennedy PG (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248. https://doi.org/10.1016/j.funeco.2015.06.006
Ochoa-Chacón A, Ramos-Valdivia AC, Poggi-Varaldo HM, Villa-Tanaca L, Martinez A, Ponce-Noyola T (2022) Fermentation performance of a mexican native Clavispora lusitaniae strain for xylitol and ethanol production from xylose, glucose and cellobiose. Enzym Microb Technol 160:110094. https://doi.org/10.1016/j.enzmictec.2022.110094
Paulson JN, Stine OC, Bravo HC, Pop M (2013) Differential abundance analysis for microbial marker-gene surveys. Nat Methods 10:1200–1202. https://doi.org/10.1038/nmeth.2658
Peng Q, Jiang S, Chen J, Ma C, Huo D, Shao Y, Zhang J (2018) Unique microbial diversity and metabolic pathway features of fermented vegetables from Hainan, China. Front Microbiol 9:399. https://doi.org/10.3389/fmicb.2018.00399
Rajkowska K, Kunicka-Styczyńska A (2018) Typing and virulence factors of food-borne Candida spp. isolates. Int J Food Microbiol 279:57–63. https://doi.org/10.1016/j.ijfoodmicro.2018.05.002
Regnat K, Mach R, Mach-Aigner A (2018) Erythritol as sweetener—wherefrom and where to? Appl Microbiol Biotechnol 102:587–595. https://doi.org/10.1007/s00253-017-8654-1
Ren F, Yan DH, Liu Y, Wang C, Guo C (2021) Bacterial and fungal communities of traditional fermented chinese soybean paste (Doujiang) and their properties. Food Sci Nutr 9:5457–5466. https://doi.org/10.1002/fsn3.2505
Sakandar HA, Usman K, Imran M (2018) Isolation and characterization of gluten-degrading Enterococcus mundtii and Wickerhamomyces anomalus, potential probiotic strains from indigenously fermented sourdough (Khamir). LWT 91:271–277. https://doi.org/10.1016/j.lwt.2018.01.023
Sakandar HA, Hussain R, Khan QF, Zhang H (2020) Functional microbiota in chinese traditional Baijiu and Mijiu Qu (starters): a review. Food Res Int 138:109830. https://doi.org/10.1016/j.foodres.2020.109830
Saran S, Mukherjee S, Dalal J, Saxena RK (2015) High production of erythritol from Candida sorbosivorans SSE-24 and its inhibitory effect on biofilm formation of Streptococcus mutans. Bioresour Technol 198:31–38. https://doi.org/10.1016/j.biortech.2015.08.146
Sharma R, Garg P, Kumar P, Bhatia SK, Kulshrestha S (2020) Microbial fermentation and its role in quality improvement of fermented foods. Fermentation 6:106. https://doi.org/10.3390/fermentation6040106
Sun H, Liu X, Wang L, Sang Y, Sun J (2022) Exploring the fungal community and its correlation with the physicochemical properties of Chinese traditional fermented fish (Suanyu). Foods 11:1721. https://doi.org/10.3390/foods11121721
Tamang JP, Shin DH, Jung SJ, Chae SW (2016) Functional properties of microorganisms in fermented foods. Front Microbiol 7:578. https://doi.org/10.3389/fmicb.2016.00578
Trindade RC, Resende MA, Silva CM, Rosa CA (2002) Yeasts associated with fresh and frozen pulps of Brazilian tropical fruits. Syst Appl Microbiol 25:294–300. https://doi.org/10.1078/0723-2020-00089
Wada K, Fujii T, Akita H, Matsushika A (2020) IoGAS1, a GPI-anchored protein derived from Issatchenkia orientalis, confers tolerance of Saccharomyces cerevisiae to multiple acids. Appl Biochem Biotechnol 190:1349–1359. https://doi.org/10.1007/s12010-019-03187-8
Wang C, Zhang Q, He L, Li C (2020) Determination of the microbial communities of Guizhou Suantang, a traditional Chinese fermented sour soup, and correlation between the identified microorganisms and volatile compounds. Food Res Int 138:109820. https://doi.org/10.1016/j.foodres.2020.109820
Wang Y, She M, Guo Z, Shuang Q (2020) Determination of fungal diversity of acidic gruel by using culture-dependent and independent methods. Food Sci Nutr 8:5832–5840. https://doi.org/10.1002/fsn3.1844
Wang J, Zhao M, Xie N, Huang M, Feng Y (2022) Community structure of yeast in fermented soy sauce and screening of functional yeast with potential to enhance the soy sauce flavor. Int J Food Microbiol 370:109652. https://doi.org/10.1016/j.ijfoodmicro.2022.109652
Xu X, Wu B, Zhao W, Lao F, Chen F, Liao X, Wu J (2021) Shifts in autochthonous microbial diversity and volatile metabolites during the fermentation of chili pepper (Capsicum frutescens L). Food Chem 335:127512. https://doi.org/10.1016/j.foodchem.2020.127512
Yan P, Jia J, Zhao H, Wu C (2022) Changes and driving mechanism of microbial community structure during paocai fermentation. Fermentation 8:281. https://doi.org/10.3390/fermentation8060281
Yang Y, Fan Y, Li T, Yang Y, Zeng F, Wang H, Zhang Y (2022) Microbial composition and correlation between microbiota and quality-related physiochemical characteristics in chongqing radish paocai. Food Chem 369:130897. https://doi.org/10.1016/j.foodchem.2021.130897
Zhang Y, Zeng T, Wang H, Song J, Suo H (2021) Correlation between the quality and microbial community of natural-type and artificial-type Yongchuan Douchi. LWT 140:110788. https://doi.org/10.1016/j.lwt.2021.111873
Zheng (2017) The effects of lactic acid bacteria isolated from Dross vinega on the growth, innate immunity of the brown-marbled grouper Epinephelus fuscoguttatus and white shrimp Litopenaeus vannamei. Dissertation, Hainan University [in Chinese]
Zhong A, Chen W, Duan Y, Li K, Tang X, Tian X, Wang C (2021) The potential correlation between microbial communities and flavors in traditional fermented sour meat. LWT 149:111873. https://doi.org/10.1016/j.lwt.2021.111873
Zhu W, He Q, Gao H, Nitayavardhana S, Khanal SK, Xie L (2020) Bioconversion of yellow wine wastes into microbial protein via mixed yeast-fungus cultures. Bioresour Technol 299:122565. https://doi.org/10.1016/j.biortech.2019.122565
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This work was supported by [Hainan Provincial Natural Science Foundation of China] (Grant numbers [322QN308]). Author Lin Huang has received this research funding.
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All authors contributed to the study’s conception and design. Lin Huang performed the study and wrote the article draft. Xinjun Chen is responsible for the concept and design of the study. Yalin Han prepared the material, and Keyan Zhong contributed significantly to data analyses and language editing. All authors read and approved the final manuscript.
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Huang, L., Han, Y., Zhong, K. et al. Exploring the fungal communities and their correlation with the physicochemical properties of Zaopocu, a distinctive fermented food on Hainan island. Biologia 78, 2593–2610 (2023). https://doi.org/10.1007/s11756-023-01407-5
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DOI: https://doi.org/10.1007/s11756-023-01407-5