Fungal diversity rather than bacterial diversity drives the ecosystem multifunctionality of vineyards in a semi-arid region
Keywords:
microbial diversity, multifunctionality, terroir, wine quality, wine sub-regionsAbstract
The presence of multiple ecosystem functions and services (i.e., ecosystem multifunctionality) has been proven to be maintained by biodiversity in natural terrestrial ecosystems. However, the mechanisms by which microbial diversity drives ecosystem functions in vineyards and the effects of ecosystem functions on wine quality remain unknown. Here, fifteen vineyards from five wine sub-regions (Shizuishan, Yinchuan, Yuquanying, Qingtongxia, and Hongsipu) in Ningxia were selected to assess the microbial community structure, ecosystem multifunctionality, and wine quality. Overall, each index differed among the vineyards from these five wine sub-regions in Ningxia. High-throughput sequencing revealed that bacterial and fungal communities varied among these vineyards. Bacterial communities were dominated by Actinobacteria, Proteobacteria, Chloroflexi, and Acidobacteria. Ascomycota was the dominant fungal phylum, followed by Basidiomycota and Mortierellomycota. In addition, fungal Shannon diversity rather than bacterial Shannon diversity showed a positive relationship with ecosystem multifunctionality. Correlation analysis revealed that ecosystem multifunctionality was positively correlated with wine acidity and negatively correlated with pH value and residual sugar content of wine. Soil chemical functions exhibited relationships with wine quality being similar to those of ecosystem multifunctionality; i.e., positively related to wine acidity but negatively related to wine pH and residual sugar content. However, soil physical functions were negatively correlated with the alcohol and anthocyanin content of wine. The research results show that the ecosystem functions maintained by fungal diversity could be attributed to wine quality of vineyards. Keywords: microbial diversity, multifunctionality, terroir, wine quality, wine sub-regions DOI: 10.25165/j.ijabe.20211406.5560 Citation: Duan B B, Ren Y Z, Zhang L Q, Suzhou C X, Chen G Q, Cui P, et al. Fungal diversity rather than bacterial diversity drives the ecosystem multifunctionality of vineyards in a semi-arid region. Int J Agric & Biol Eng, 2021; 14(6): 126–136.References
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[43] Govaerts B, Mezzalama M, Unno Y, Sayre K D, Luna-Guido M, Vanherck K, et al. Influence of tillage, residue management, and crop rotation on soil microbial biomass and catabolic diversity. Applied Soil Ecology, 2007; 37: 18–30.
[44] Ochoa‐Hueso R, Eldridge D J, Delgado‐Baquerizo M, Soliveres S, Bowker M A, Gross N, et al. Soil fungal abundance and plant functional traits drive fertile island formation in global drylands. Journal of Ecology, 2017; 106(1): 242–253.
[45] Koundouras S, Hatzidimitriou E, Karamolegkou M, Dimopoulou E, Kallithraka S, Tsialtas J T, et al. Irrigation and rootstock effects on the phenolic concentration and aroma potential of Vitis vinifera L. cv. Cabernet Sauvignon grapes. Journal of Agricultural and Food Chemistry, 2009; 57(17): 7805–7813.
[46] Tongsiri P, Tseng W Y, Shen Y, Lai H Y. Comparison of soil properties and organic components in infusions according to different aerial appearances of tea plantations in Central Taiwan. Sustainability, 2020; 12: 4384. doi: 10.3390/su12114384.
[2] van der Plas F, Manning P, Soliveres S, Allan E, Scherer-Lorenzen M, Verheyen K, et al. Biotic homogenization can decrease landscape-scale forest multifunctionality. Proceedings of the National Academy of Sciences of the United States of America, 2016; 113(13): 3557–3562.
[3] Delgado‐Baquerizo M, Trivedi P, Trivedi C, Eldridge D J, Reich P B, Jeffries T C, et al. Microbial richness and composition independently drive soil multifunctionality. Functional Ecology, 2017; 31(12): 2330–2343.
[4] Sharafatmandrad M, Mashizi A K. Investigating distribution of ecosystem services in rangeland landscapes: an approach based on weighted key functional traits. Ecological Indicators, 2020; 111: 105971. doi: 10.1016/j.ecolind.2019.105971.
[5] Birkhofer K, Andersson G K S, Bengtsson J, Bommarco R, Dänhardt J, Ekbom B, et al. Relationships between multiple biodiversity components and ecosystem services along a landscape complexity gradient. Biological Conservation, 2018; 218: 247–253.
[6] Schuldt A, Assmann T, Brezzi M, Buscot F, Eichenberg D, Gutknecht J, et al. Biodiversity across trophic levels drives multifunctionality in highly diverse forests. Nature Communications, 2018; 9: 2989. doi: 10.1038/ s41467-018-05421-z.
[7] Wang L, Delgado-Baquerizo M, Wang D, Isbell F, Liu J, Feng C, et al. Diversifying livestock promotes multidiversity and multifunctionality in managed grasslands. Proceedings of the National Academy of Sciences of the United States of America, 2019; 116: 6187–6192.
[8] Griggs R G, Steenwerth K L, Mills D A, Cantu D, Bokulich N A. Sources and assembly of microbial communities in vineyards as a functional component of winegrowing. Frontiers in Microbiology, 2021; 12: 673810. doi: 10.3389/fmicb.2021.673810.
[9] Isbell F, Calcagno V, Hector A, Connolly J, Harpole W S, Reich P B, et al. High plant diversity is needed to maintain ecosystem services. Nature, 2011; 477: 199–202. doi: 10.1038/nature10282.
[10] Jing X, Sanders N J, Shi Y, Chu H, Classen A T, Zhao K, et al. The links between ecosystem multifunctionality and above- and belowground biodiversity are mediated by climate. Nature Communications, 2015; 6: 8159. doi: 10.1038/ncomms9159.
[11] Li J, Delgado-Baquerizo M, Wang J T, Hu H W, Cai Z J, Zhu Y N, et al. Fungal richness contributes to multifunctionality in boreal forest soil. Soil Biology and Biochemistry, 2019; 136: 107526. doi: 10.1016/ j.soilbio.2019.107526.
[12] Chen Q L, Ding J, Li C Y, Yan Z Z, He J Z, Hu H W. Microbial functional attributes, rather than taxonomic attributes, drive top soil respiration, nitrification and denitrification processes. Science of the Total Environment, 2020; 734: 139479. doi: 10.1016/j.scitotenv.2020. 139479.
[13] Chen Q L, Ding J, Zhu D, Hu H W, Delgado-Baquerizo M, Ma Y B, et al. Rare microbial taxa as the major drivers of ecosystem multifunctionality in long-term fertilized soils. Soil Biology and Biochemistry, 2020; 141: 107686. doi: 10.1016/j.soilbio.2019.107686.
[14] Wang X Q, Chen X B, Zhan J C, Huang W D. Effects of ecological factors on quality of winegrape and wine. Food Science, 2006; 27: 791–797.
[15] Shi P B, Chen H J, Zhang Z W. Chemical and physical properties of soils in hillside vineyards at different altitudes. Soil, 2009; 41: 495–499.
[16] Miele A, Rizzon L A. Rootstock-scion interaction: 2. Effect on the composition of Cabernet Sauvignon grape must. Revista Brasileira de Fruticultura, 2017; 39. doi: 10.1590/0100-29452017434.
[17] Reynolds A G, Taylor G, de Savigny C. Defining Niagara terroir by chemical and sensory analysis of Chardonnay wines from various soil textures and vine sizes. American Journal of Enology and Viticulture, 2013; 64: 180–194.
[18] Cortell J M, Halbleib M, Gallagher A V, Righetti T L, Kennedy J A. Influence of vine vigor on grape (Vitis vinifera L. cv. Pinot noir) and wine proanthocyanidins. Journal of Agricultural and Food Chemistry, 2005; 53: 5798–5808.
[19] Tardaguila J, Baluja J, Arpon L, Balda P, Oliveira M. Variations of soil properties affect the vegetative growth and yield components of “Tempranillo” grapevines. Precision Agriculture, 2011; 12: 762–773.
[20] Perkins V P. Growth and rippening of strawberry fruit. Horticultural Reviews, 1995; 17: 267–297.
[21] Zhang Z, Li H, Zhang J, Xue J, Zhang X J. Aroma characteristics of aged ‘Cabernet Sauvignon’ dry red wine from eastern foothill of Helan mountain. Food Science, 2019; 40(18): 203–209. (in Chinese)
[22] Bremner J M, Mulvaney C S. “Nitrogen-Total” in Methods of soil analysis. Part 2. chemical and microbiological properties. eds. A. L. Page, R. H. Miller, and D. R. Keeney, American Society of Agronomy, Soil Science Society of America, Madison, Wisconsin, 1982; pp.595–624.
[23] Schade J D, Kyle M, Hobbie S E, Fagan W F, Elser J J. Stoichiometric tracking of soil nutrients by a desert insect herbivore. Ecology Letters, 2003; 6: 96–101.
[24] Wang H. Wine analysis and determination. Beijing: China Agriculture Press, 2011; pp.118–135. (in Chinese)
[25] Kim D O, Chun O K, Kim Y J, Moon H Y, Lee C Y. Quantification of polyphenolics and their antioxidant capacity in fresh plums. Journal of Agricultural and Food Chemistry, 2003; 51(22): 6509–6515.
[26] Cliff M A, King M C, Schlosser J. Anthocyanin, phenolic composition, colour measurement and sensory analysis of BC commercial red wines. Food Research International, 2007; 40(1): 92–100.
[27] Caporaso J G, Kuczynski J, Stombaugh J, Bittinger K, Bushman F D, Costello E K, et al. QIIME allows analysis of high-throughput community sequencing data. Nature Biotechnology, 2010; 7: 335–336.
[28] Byrnes J E K, Gamfeldt L, Isbell F, Lefcheck J S, Griffin J N, Hector A, et al. Investigating the relationship between biodiversity and ecosystem multifunctionality: challenges and solutions. Methods in Ecology and Evolution, 2014; 5: 111–124. doi: 10.1111/2041-210X.12143.
[29] Lefcheck J S, Byrnes J E K, Isbell F, Gamfeldt L, Griffin J N, Eisenhauer N, et al. Biodiversity enhances ecosystem multifunctionality across trophic levels and habitats. Nature Communications, 2015; 6: 6936. doi: 10.1038/ncomms7936.
[30] Perkins D M, Bailey R A, Dossena M, Gamfeldt L, Reiss J, Trimmer M, et al. Higher biodiversity is required to sustain multiple ecosystem processes across temperature regimes. Global Change Biology, 2015; 21(1): 396–406.
[31] Valencia E, Maestre F T, Le Bagousse-Pinguet Y, Quero J L, Tamme R, Borger L, et al. Functional diversity enhances the resistance of ecosystem multifunctionality to aridity in Mediterranean drylands. New Phytologist, 2015; 206: 660–671.
[32] Maestre F T, Quero J L, Gotelli N J, Escudero A, Ochoa V, Delgado-Baquerizo M, et al. Plant species richness and ecosystem multifunctionality in global drylands. Science, 2012; 335: 214–218.
[33] Wang W, Buligen J, Hu X D, Xia J F, Zhang Z D, Gu M Y, et al. Analysis of the microbial community diversity of soil from wine grape productiing area in Xinjiang based on high-throughput sequencing. Xinjiang Agriculture Science, 2020; 57: 859–868. (in Chinese)
[34] Wei Y J, Zhou W, Ma W R. Microbial diversity of berries, leaves and soil of grapevine plants grown in Xinjiang analyzed by high-throughput sequencing. Food Science, 2018; 39(6): 162–170. (in Chinese)
[35] Leff J W, Jones S E, Prober S M, Barberan A, Borer E T, Firn J L, et al. Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proceedings of the National Academy of Sciences of the United States of America, 2015; 112: 10967–10972.
[36] Blackwood C B, Waldrop M P, Zak D R, Sinsabaugh R L. Molecular analysis of fungal communities and laccase genes in decomposing litter reveals differences among forest types but no impact of nitrogen deposition. Environmental Microbiology, 2007; 9(5): 1306–1316.
[37] Curlevski N J A, Xu Z, Anderson I C, Cairney J W G. Converting Australian tropical rainforest to native Araucariaceae plantations alters soil fungal communities. Soil Biology and Biochemistry, 2010; 42(1): 14–20.
[38] Tan Y, Cui Y, Li H, Kuang A, Li X, Wei Y, et al. Rhizospheric soil and root endogenous fungal diversity and composition in response to continuous Panax notoginseng cropping practices. Microbiological Research, 2017; 194: 10–19.
[39] Cordero-Bueso G, Arroyo T, Serrano A, Tello J, Aporta I, Velez M D, et al. Influence of the farming system and vine variety on yeast communities associated with grape berries. International Journal of Food Microbiology, 2011; 145(1): 132–139.
[40] Xu W, Ma Z, Jing X, He J S. Biodiversity and ecosystem multifunctionality: advances and perspectives. Biodiversity Science, 2016; 24(1): 55–71.
[41] Miki T, Yokokawa T, Matsui K. Biodiversity and multifunctionality in a microbial community: a novel theoretical approach to quantify functional redundancy. Proceedings of the Royal Society of London, Series B: Biological Sciences, 2014; 281: 20132498. doi: 10.1098/rspb.2013.2498.
[42] Tsiafouli M A, Thebault E, Sgardelis S P, de Ruiter P C, van der Putten W H, Birkhofer K, et al. Intensive agriculture reduces soil biodiversity across Europe. Global Change Biology, 2015; 21(2): 973–985.
[43] Govaerts B, Mezzalama M, Unno Y, Sayre K D, Luna-Guido M, Vanherck K, et al. Influence of tillage, residue management, and crop rotation on soil microbial biomass and catabolic diversity. Applied Soil Ecology, 2007; 37: 18–30.
[44] Ochoa‐Hueso R, Eldridge D J, Delgado‐Baquerizo M, Soliveres S, Bowker M A, Gross N, et al. Soil fungal abundance and plant functional traits drive fertile island formation in global drylands. Journal of Ecology, 2017; 106(1): 242–253.
[45] Koundouras S, Hatzidimitriou E, Karamolegkou M, Dimopoulou E, Kallithraka S, Tsialtas J T, et al. Irrigation and rootstock effects on the phenolic concentration and aroma potential of Vitis vinifera L. cv. Cabernet Sauvignon grapes. Journal of Agricultural and Food Chemistry, 2009; 57(17): 7805–7813.
[46] Tongsiri P, Tseng W Y, Shen Y, Lai H Y. Comparison of soil properties and organic components in infusions according to different aerial appearances of tea plantations in Central Taiwan. Sustainability, 2020; 12: 4384. doi: 10.3390/su12114384.
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2021-12-16
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Duan, B., Ren, Y., Zhang, L., Suzhou, C., Chen, G., Cui, P., … Liu, X. (2021). Fungal diversity rather than bacterial diversity drives the ecosystem multifunctionality of vineyards in a semi-arid region. International Journal of Agricultural and Biological Engineering, 14(6), 126–136. Retrieved from https://ijabe.migration.pkpps03.publicknowledgeproject.org/index.php/ijabe/article/view/5560
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