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The Biogeography of Fungal Communities Across Different Chinese Wine-Producing Regions Associated with Environmental Factors

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The Biogeography of Fungal Communities Across Different Chinese Wine-Producing Regions Associated with Environmental Factors bioRxiv preprint doi: https://doi.org/10.1101/2020.10.22.351585; this version posted October 23, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 The Biogeography of Fungal Communities Across Different Chinese Wine- 2 producing Regions Associated with Environmental Factors and Spontaneous 3 Fermentation Performance 4 Ruilong Li,a Siyu Yang,a Mengyuan Lin,a Sijiang Guo,a Xiaoyu Han,a Mengmeng Ren,a Le 5 Du,b Yinghui Song,c Yilin You,a Jicheng Zhan,a# Weidong Huang,a# 6 aCollege of Food Science and Nutritional Engineering, Beijing Key Laboratory of Viticulture 7 and Enology, China Agricultural University, Beijing, 100083, China 8 bWuhan Donghu Big Data Trading Center Co. Ltd., Wuhan, 430200, China 9 cPenglai Grape and Wine Industry Development Service Center, Yantai, 265600, China 10 #Address correspondence to Weidong Huang, [email protected]; Jicheng 11 Zhan,[email protected]. 12 Abstract Chinese Marselan grapes are believed to possess the potential to become a characteristic 13 regional variety, whose quality is internationally recognized. The fermentation-related mycobiota 14 from six climatically diverse Marselan-producing regions in China were analyzed via high- 15 throughput sequencing (HTS), while the influence of environmental factors was evaluated as well. 16 The results implied that the phyla Ascomycota and genus Aureobasidium dominated the fungal 17 communities in 166 Marselan must and ferment samples. Significant differences were detected in 18 the fungal microbiota from the regions, as well as the wineries, while these discrepancies decreased 19 as the fermentation progressed. Moreover, the difference in fungal communities between the bioRxiv preprint doi: https://doi.org/10.1101/2020.10.22.351585; this version posted October 23, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 20 wineries exceeded the variation involving the regions, and higher diversity was identified in the 21 types of species than in the compositions. Geoclimatic elements (Gc) and physicochemical indexes 22 (Pi) exerted a significant effect on the fungal must consortium, explaining 58.17% of the 23 taxonomic information. Therefore, a correlation was proposed between the spontaneous 24 fermentation performance, as well as the polyphenol (PP) content, and their association with fungal 25 taxonomic composition. In addition to enriching the knowledge regarding the wine microbiome 26 and its influencing factors, this study may provide a new strategy for harnessing autochthonous 27 “microbial terroir”. 28 Importance Wine microbiome and their metabolism play a crucial role in wine quality. Chinese 29 wine-producing regions are widely distributed with diverse geoclimatic conditions, this study 30 reports a most comprehensive biogeography of fermentation-related fungal communities 31 performed to date, taking the Chinese promising Marselan grape variety as the research object. It 32 reveals significant differences in the fungal microbiota of Marselan must and ferment from 33 different regions and wineries, and higher otherness between species type than that between 34 species composition. The study also reports the main geoclimatic and physicochemical factors 35 shaping fungal flora. Moreover, a correlation was proposed among the spontaneous fermentation 36 performance with fungal taxonomic composition and polyphenol content. Taken together, the 37 results shed light on the wine fungal communities and its influencing factors, which is crucial for 38 vineyard and fermentation microorganism management, and may also provide a new strategy for 39 harnessing autochthonous “microbial terroir” by utilizing spontaneous fermentation. 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.22.351585; this version posted October 23, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 40 Keywords Marselan, fungal community, high-throughput sequencing, spontaneous fermentation, 41 geoclimatic element 42 Introduction 43 The process of wine fermentation harbors a complex microbiome (1), and their metabolism 44 plays a crucial role in wine quality (2). Although various fungi and bacteria colonize the roots, 45 stems, leaves, flowers, and fruits of grapevines, most grape fruit-related microorganisms are unable 46 to survive during the wine fermentation process (3), due to stress factors such as high ethanol 47 concentrations , low pH, and anaerobic environments (4). Compared with bacteria, the 48 fermentation process has a more substantial impact on the fungal flora (5), while the fungal must 49 consortium displays higher annual stability (6). As the core microorganisms of alcohol 50 fermentation, yeasts have a significant influence on the flavor and quality of wine (7), but since 51 the microbial consortia of wine fermentation is a complex ecosystem with sophisticated 52 interactions (8), these considerations mandate an integral understanding of fungal communities 53 during wine fermentation (9). With the development of gene sequencing technology, several 54 studies have documented the fungal microbiota related to wine fermentation worldwide (6, 10, 11). 55 HTS has been widely used in fungal diversity research and has been proven an effective method 56 for studying microorganisms during fermentation (12). 57 As a product with both cultural and economic value, wine is appreciated for its regional 58 differences, also known as terroir (13). Previously, wine terroir was attributed to the soil and the 59 vineyard environment, and the concept of “microbial terroir” was presented in conjunction with 60 the development of microbial wine research (14). The distribution of Chinese wine-producing 61 regions is extensive, covering 179 counties, with a range of 24-47 °N latitude (LAT) and 76-132 °E 62 longitude (LNT). Significant differences in climate are evident between the producing regions, and 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.22.351585; this version posted October 23, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 63 various microclimates exist in each area (15). To date, research in China has focused on partial 64 regions (16, 17), and knowledge regarding the fungal microbiome exposed to different climatic 65 conditions nationwide remains minimal (9, 17-19). 66 Since being introduced into China in 2001, and due to its excellent adaptability and 67 fermentative characteristics, the planting area of Marselan has gradually expanded. At present, 68 China is one of the countries with the largest Marselan planting area (20). The flavor and quality 69 of wine produced from Marselan are exceedingly popular with consumers and experts both 70 domestically and abroad, and it is expected to become a representative variety of the Chinese wine 71 industry (21). As an emerging variety, current studies primarily focus on its fermentation and 72 cultivation (22), and information regarding the fungal consortium during the fermentation process 73 of Marselan grape from different regions is scarce (23). 74 In this study, the fungal communities of the must and ferment from six major Marselan 75 regions (fifteen wineries) in China are assessed via HTS analysis for internal transcribed spacer II 76 (ITS2) genes. Furthermore, coordinate and cluster analysis are applied to test the fungal 77 community homeomorphism among regions and wineries. In addition, correlation analysis is used 78 to explore the relationship between the fungal consortium and geoclimatic factors, as well as the 79 influence of fungal composition on the physicochemical indexes of spontaneously fermented wine. 80 In conclusion, we conduct a systematic study to uncover the fungal communities and its 81 influencing factors in different Marselan producing regions. 82 Results 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.22.351585; this version posted October 23, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 83 Taxonomic Assignment and α-diversity Analysis of Marselan Fungal Communities 84 Marselan grapes from fifteen different wineries in the six main Chinese producing regions were 85 collected, and spontaneous fermentation was carried out to investigate the fungal consortium in 86 Marselan must and ferment. Supplementary Table S1 shows the sampling of the wineries and 87 regions. During the fermentation process, 1611 operational taxonomic units (OTUs) with 97% 88 similarity were observed in 166 samples with average ITS2 rDNA reads of 80,055 (Supplementary 89 Dataset S1). Compared with the fungal reference database, taxonomic assignment revealed at least 90 three fungal phyla (Ascomycota, Basidiomycota and Mucoromycota),
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