异常威克汉姆酵母对采后桃果表面微生物动态的影响机制

摘要/Abstract

摘要： 果实表面定殖着复杂的微生物群落，其结构易受采后处理的影响，进而改变果实的贮藏与保鲜。已有研究表明，异常威克汉姆酵母能有效防控桃果采后病害，但其生物防治机制尚未明确。为此，本研究从分子层面探讨了该酵母对桃果表面微生物群落的影响。结果表明，异常威克汉姆酵母处理可显著降低桃果贮藏期间的自然腐烂率（降幅达38.88%），并维持果实品质和营养稳定。该处理提高了细菌群落的多样性和丰富度，降低了真菌群落的多样性与丰富度，且对真菌群落结构的重组作用尤为显著。异常威克汉姆酵母通过建立优势地位和抑制主要致病菌如链格孢菌、镰刀菌、枝孢霉的生长，重塑果实微生物群落组成。此外，处理促进了如假单胞菌、甲基杆菌-甲基红色杆菌、短小杆菌、薄层菌等有益细菌属，以及戈卢别夫氏酵母、枝顶孢霉等有益真菌类群的动态演替进程。以上结果说明，异常威克汉姆酵母通过直接抑制病原真菌并系统调控微生物群落结构，实现了对桃果采后腐烂的协同防控。

关键词: 梨果, 异常威克汉姆酵母, 采后, 细菌群落, 真菌群落

Abstract: The surfaces of fruit harbor complex microbial communities, the structure of which can be significantly altered by postharvest treatments, ultimately affecting storage performance and shelf life. While Wickerhamomyces anomalus has been shown to effectively control postharvest diseases in peach fruit, its underlying biocontrol mechanisms remain unclear. To address this, we investigated how this yeast influences the peach surface microbiome at a molecular level. Our results demonstrate that W. anomalus treatment significantly suppressed natural decay during storage, reducing the decay rate by 38.88% while preserving fruit quality and nutritional stability. The treatment increased the diversity and richness of the bacterial community but decreased those of the fungal community, with particularly strong restructuring effects on fungal composition. W. anomalus reconfigured the microbiome by establishing dominance and suppressing key pathogenic fungi such as Alternaria, Cladosporium, and Fusarium. Furthermore, the treatment reversed the successional dynamics of beneficial bacterial genera, including Pseudomonas, Methylobacterium-Methylorubrum, Curtobacterium, and Hymenobacter, as well as fungal taxa such as Golubevia and Acremonium. These findings indicate that W. anomalus achieves synergistic control of postharvest decay in peach fruit through direct suppression of pathogenic fungi and systematic modulation of the microbial community structure.

Key words: Peach, Wickerhamomyces anomalus, Postharvest, Bacterial community, Fungal community

中图分类号:

TS201.3

陈夕飞周娅丽何雨洁 Solairaj Dhanasekaran 李军张晓云赵利娜张红印. 异常威克汉姆酵母对采后桃果表面微生物动态的影响机制[J]. 食品科学.

Xifei Chen. Biocontrol Mechanism of Wickerhamomyces anomalus: Influencing Microbial Dynamics on the Surface of Postharvest Peaches[J]. FOOD SCIENCE.

参考文献

[1] CHEN M J, JIA F, CHEN S, et al. Streptomyces virginiae XDS1-5, an antagonistic actinomycete, as a biocontrol to peach brown rot caused by Monilinia fructicola[J]. Journal of the Science of Food and Agriculture, 2024, 104(12): 7514-7523. DOI:10.1002/jsfa.13573.
[2] TSALGATIDOU P C, PAPAGEORGIOU A, BOUTSIKA A, et al. Insights into the Interaction between the Biocontrol Agent Bacillus amyloliquefaciens QST 713, the Pathogen Monilinia fructicola and Peach Fruit[J]. Agronomy-Basel, 2024, 14. DOI:10.3390/agronomy14040771.
[3] ZHAO Q H, SHI Y, NGEA G L N, et al. Changes of the microbial community in kiwifruit during storage after postharvest application of Wickerhamomyces anomalus[J]. Food Chemistry, 2023, 404. DOI:10.1016/j.foodchem.2022.134593.
[4] ZHOU T, SCHNEIDER K E, LI X Z. Development of biocontrol agents from food microbial isolates for controlling post-harvest peach brown rot caused by Monilinia fructicola[J]. International Journal of Food Microbiology, 2008, 126(1-2): 180-185. DOI:10.1016/j.ijfoodmicro.2008.05.020.
[5] ZHANG Q R, ZHAO L N, LI Z B, et al. Screening and identification of an antagonistic yeast controlling postharvest blue mold decay of pears and the possible mechanisms involved[J]. Biological Control, 2019, 133: 26-33. DOI:10.1016/j.biocontrol.2019.03.002.
[6] ZHANG X K, LI B Q, ZHANG Z Q, et al. Antagonistic Yeasts: A Promising Alternative to Chemical Fungicides for Controlling Postharvest Decay of Fruit[J]. Journal of Fungi, 2020, 6. DOI:10.3390/jof6030158.
[7] KUSSTATSCHER P, CERNAVA T, ABDELFATTAH A, et al. Microbiome approaches provide the key to biologically control postharvest pathogens and storability of fruits and vegetables[J]. Fems Microbiology Ecology, 2020, 96(7). DOI:10.1093/femsec/fiaa119.
[8] MüLLER D B, VOGEL C, BAI Y, et al. Annual Review of Genetics[M]. Palo Alto: Annual Reviews, 2016, 50: 211-234. https://doi.org/10.1146/annurev-genet-120215-034952.
[9] LIU X, GAO Y, YANG H Y, et al. Pichia kudriavzevii retards fungal decay by influencing the fungal community succession during cherry tomato fruit storage[J]. Food Microbiology, 2020, 88: 103404. DOI:10.1016/j.fm.2019.103404.
[10] SHEN Y M, LI X N, XIONG R, et al. Effect of peach trichome removal on post-harvest brown rot and on the fruit surface microbiome[J]. International Journal of Food Microbiology, 2023, 402: 110299. DOI:10.1016/j.ijfoodmicro.2023.110299.
[11] SHI Y, YANG Q Y, ZHAO Q H, et al. Aureobasidium pullulans S-2 reduced the disease incidence of tomato by influencing the postharvest microbiome during storage[J]. Postharvest Biology and Technology, 2022, 185. DOI:10.1016/j.postharvbio.2021.111809.
[12] ZHAO L A, ZHOU Y L, LIANG L Y, et al. Changes in quality and microbiome composition of strawberry fruits following postharvest application of Debaryomyces hansenii, a yeast biocontrol agent[J]. Postharvest Biology and Technology, 2023, 202. DOI:10.1016/j.postharvbio.2023.112379.
[13] ZHAO L A, ZHOU Y L, LIANG L Y, et al. Proteomic analysis reveals the mechanisms of improved biocontrol efficacy of Sporidiobolus pararoseus Y16 induced by γ-aminobutyric acid[J]. Biological Control, 2023, 185. DOI:10.1016/j.biocontrol.2023.105313.
[14] IKHAJIAGBE B, OGWU M C, FAWEHINMI F O, et al. Comparative growth responses of Amaranthus [L.] species in Humus and Ferruginous Ultisols using plant growth promoting Rhizobacteria (Pseudomonas species)[J]. South African Journal of Botany, 2021, 137: 10-18. DOI:10.1016/j.sajb.2020.09.029.
[15] KURNIAWAN O, WILSON K, MOHAMED R, et al. Bacillus and Pseudomonas spp. provide antifungal activity against gray mold and Alternaria rot on blueberry fruit[J]. Biological Control, 2018, 126: 136-141. DOI:10.1016/j.biocontrol.2018.08.001.
[16] WANG Z R, ZHONG T, CHEN X H, et al. Multiple pre-harvest applications of antagonist Pseudomonas fluorescens ZX induce resistance against blue and green molds in postharvest citrus fruit[J]. Lwt-Food Science and Technology, 2022, 155. DOI:10.1016/j.lwt.2021.112922.
[17] AIELLO D, RESTUCCIA C, STEFANI E, et al. Postharvest biocontrol ability of Pseudomonas synxantha against Monilinia fructicola and Monilinia fructigena on stone fruit[J]. Postharvest Biology and Technology, 2019, 149: 83-89. DOI:10.1016/j.postharvbio.2018.11.020.
[18] VANACORE A, FORGIONE M C, CAVASSO D, et al. Role of EPS in mitigation of plant abiotic stress: The case of Methylobacterium extorquens PA1[J]. Carbohydrate Polymers, 2022, 295. DOI:10.1016/j.carbpol.2022.119863.
[19] KRISHNAMOORTHY A, AGARWAL T, KOTAMREDDY J N R, et al. Impact of seed-transmitted endophytic bacteria on intra- and inter-cultivar plant growth promotion modulated by certain sets of metabolites in rice crop[J]. Microbiological Research, 2020, 241. DOI:10.1016/j.micres.2020.126582.
[20] JORGE G L, KISIALA A, MORRISON E, et al. Endosymbiotic Methylobacterium oryzae mitigates the impact of limited water availability in lentil (Lens culinaris Medik.) by increasing plant cytokinin levels[J]. Environmental and Experimental Botany, 2019, 162: 525-540. DOI:10.1016/j.envexpbot.2019.03.028.
[21] PUGAZHENDHI A, RADHAKRISHNAN R, DUC P A. Curtobacterium sp. MA01 generates oxidative stress to inhibit the plant growth[J]. Biocatalysis and Agricultural Biotechnology, 2019, 20. DOI:10.1016/j.bcab.2019.101274.
[22] SILAMBARASAN S, LOGESWARI P, VALENTINE A, et al. Role of Curtobacterium herbarum strain CAH5 on aluminum bioaccumulation and enhancement of Lactuca sativa growth under aluminum and drought stresses[J]. Ecotoxicology and Environmental Safety, 2019, 183. DOI:10.1016/j.ecoenv.2019.109573.
[23] KHLEIFAT K, MAGHARBEH M, ALQARALEH M, et al. Biodegradation modeling of phenol using Curtobacterium flaccumfaciens as plant-growth-promoting bacteria[J]. Heliyon, 2022, 8(9). DOI:10.1016/j.heliyon.2022.e10490.
[24] MASOUMI F, KHADIVINIA E, ALIDOUST L, et al. Nickel and lead biosorption by Curtobacterium sp. FM01, an indigenous bacterium isolated from farmland soils of northeast Iran[J]. Journal of Environmental Chemical Engineering, 2016, 4(1): 950-957. DOI:10.1016/j.jece.2015.12.025.
[25] SUNDARARAMAN A, DAHAL R H, KIM D U, et al. Genome Sequence of Hymenobacter polaris RP-2-7T, Isolated from Arctic Soil[J]. Microbiology Resource Announcements, 2021, 10(1): e01216-20. DOI:10.1128/mra.01216-20.
[26] SEDLáCEK I, PANTUCEK R, KRáLOVá S, et al. Hymenobacter amundsenii sp. nov. resistant to ultraviolet radiation, isolated from regoliths in Antarctica[J]. Systematic and Applied Microbiology, 2019, 42(3): 284-290. DOI:10.1016/j.syapm.2018.12.004.
[27] PARK Y H, KIM Y, MISHRA R C, et al. Fungal endophytes inhabiting mountain-cultivated ginseng (Panax ginseng Meyer): Diversity and biocontrol activity against ginseng pathogens[J]. Scientific Reports, 2017, 7: 16221. DOI:10.1038/s41598-017-16181-z.
[28] TRALAMAZZA S M, PIACENTINI K C, IWASE C H T, et al. Toxigenic Alternaria species: impact in cereals worldwide[J]. Current Opinion in Food Science, 2018, 23: 57-63. DOI:10.1016/j.cofs.2018.05.002.
[29] ALI S, TYAGI A, RAJARAMMOHAN S, et al. Revisiting Alternaria-host interactions: New insights on its pathogenesis, defense mechanisms and control strategies[J]. Scientia Horticulturae, 2023, 322: 112424. DOI:10.1016/j.scienta.2023.112424.
[30] HERNáNDEZ-TASCO A J, ALVAREZ-CANTERO C J, RAMíREZ-RUEDA R Y, et al. Endophytic fungus Cladosporium sp (AC-1) isolated from leaves of Annona cacans (Annonaceae) shows high metabolic plasticity to produce bioactive molecules[J]. Biocatalysis and Agricultural Biotechnology, 2022, 44: 102463. DOI:10.1016/j.bcab.2022.102463.
[31] SALVATORE M M, ANDOLFI A, NICOLETTI R. The Genus Cladosporium: A Rich Source of Diverse and Bioactive Natural Compounds[J]. Molecules, 2021, 26(13): 3959. DOI:10.3390/molecules26133959.
[32] DEAN R, VAN KAN J A L, PRETORIUS Z A, et al. The Top 10 fungal pathogens in molecular plant pathology[J]. Molecular Plant Pathology, 2012, 13(4): 414-430. DOI:10.1111/j.1364-3703.2011.00783.x.
[33] O'DONNELL K, WHITAKER B K, LARABA I, et al. DNA Sequence-Based Identification of Khleifat,: A Work in Progress[J]. Plant Disease, 2022, 106(6): 1597-1609. DOI:10.1094/pdis-09-21-2035-sr.
[34] BALAMURUGAN A, ASHAJYOTHI M, SHANU K, et al. Chrysanthemum wilt caused by Fusarium incarnatum: Etiology unveiled through polyphasic taxonomic methods[J]. Physiological and Molecular Plant Pathology, 2024, 129: 102214. DOI:10.1016/j.pmpp.2023.102214.
[35] MIAO W H, YANG Y R, WU M T, et al. Potential pathways and genes expressed in Chrysanthemum in response to early fusarium oxysporum infection[J]. Bmc Plant Biology, 2023, 23(1): 312. DOI:10.1186/s12870-023-04331-7.
[36] CHAI C Y, KE T, NIU Q H, et al. Diversity of Wickerhamomyces (Wickerhamomycetaceae, Saccharomycetales) in China with the description of four new species[J]. Frontiers in Microbiology, 2024, 15. DOI:10.3389/fmicb.2024.1338231.
[37] CZARNECKA M, ZAROWSKA B, POLOMSKA X, et al. Role of biocontrol yeasts Debaryomyces hansenii and Wickerhamomyces anomalus in plants' defence mechanisms against Monilinia fructicola in apple fruits[J]. Food Microbiology, 2019, 83: 1-8. DOI:10.1016/j.fm.2019.04.004.
[38] ZHAO L N, WANG Y J, DHANASEKARAN S, et al. Efficacy of Wickerhamomyces anomalus yeast in the biocontrol of blue mold decay in apples and investigation of the mechanisms involved[J]. Biocontrol, 2021, 66(4): 547-558. DOI:10.1007/s10526-021-10088-5.
[39] ZHU M R, YANG Q Y, GODANA E A, et al. Efficacy of Wickerhamomyces anomalus in the biocontrol of black spot decay in tomatoes and investigation of the mechanisms involved[J]. Biological Control, 2023, 186. DOI:10.1016/j.biocontrol.2023.105356.
[40] RAYNALDO F A, DHANASEKARAN S, NGEA G L N, et al. Investigating the biocontrol potentiality of Wickerhamomyces anomalus against postharvest gray mold decay in cherry tomatoes[J]. Scientia Horticulturae, 2021, 285: 110137. DOI:10.1016/j.scienta.2021.110137.
[41] RUSS L, LOMBAERS-VAN DER PLAS C, CASTILLO-RUSSI J D, et al. Deciphering the modes of action of Golubevia sp., an antagonist against the causal agent of powdery mildew in wheat, using an mRNA-based systems approach[J]. Biological Control, 2021, 152: 104446. DOI:10.1016/j.biocontrol.2020.104446.
[42] WICKLOW D T, ROTH S, DEYRUP S T, et al. A protective endophyte of maize: Acremonium zeae antibiotics inhibitory to Aspergillus flavus and Fusarium verticillioides[J]. Mycological Research, 2005, 109: 610-618. DOI:10.1017/s0953756205002820.
[43] LLORENS E, SCALSCHI L, SHARON O, et al. Jasmonic acid pathway is required in the resistance induced by Acremonium sclerotigenum in tomato against Pseudomonas syringae[J]. Plant Science, 2022, 318: 111210. DOI:10.1016/j.plantsci.2022.111210.
[44] WANI S M, MIR S A, KHANDAY F A, et al. Advances in pullulan production from agro-based wastes by Aureobasidium pullulans and its applications[J]. Innovative Food Science & Emerging Technologies, 2021, 74: 102846. DOI:10.1016/j.ifset.2021.102846.
[45] IPPOLITO A, EL GHAOUTH A, WILSON C L, et al. Control of postharvest decay of apple fruit by Aureobasidium pullulans and induction of defense responses[J]. Postharvest Biology and Technology, 2000, 19(3): 265-272. DOI:10.1016/s0925-5214(00)00104-6.
[46] ZHANG K, LIN C Y, ZHAO S S, et al. The role of pH transcription factor Appacc in upregulation of pullulan biosynthesis in Aureobasidium pullulans using potato waste as a substrate[J]. International Journal of Biological Macromolecules, 2023, 242: 124797. DOI:10.1016/j.ijbiomac.2023.124797.
[47] MARI M, MARTINI C, SPADONI A, et al. Biocontrol of apple postharvest decay by Aureobasidium pullulans[J]. Postharvest Biology and Technology, 2012, 73: 56-62. DOI:10.1016/j.postharvbio.2012.05.014.
[48] DI FRANCESCO A, UGOLINI L, LAZZERI L, et al. Production of volatile organic compounds by Aureobasidium pullulans as a potential mechanism of action against postharvest fruit pathogens[J]. Biological Control, 2015, 81: 8-14. DOI:10.1016/j.biocontrol.2014.10.004.
[49] MARI M, MARTINI C, GUIDARELLI M, et al. Postharvest biocontrol of Monilinia laxa, Monilinia fructicola and Monilinia fructigena on stone fruit by two Aureobasidium pullulans strains[J]. Biological Control, 2012, 60(2): 132-140. DOI:10.1016/j.biocontrol.2011.10.013.
[50] LIU S Y, XIE J G, LUAN W Q, et al. Papiliotrema flavescens, a plant growth-promoting fungus, alters root system architecture and induces systemic resistance through its volatile organic compounds in Arabidopsis[J]. Plant Physiology and Biochemistry, 2024, 208: 108474. DOI:10.1016/j.plaphy.2024.108474.
[51] SCHISLER D A, YOSHIOKA M, VAUGHAN M M, et al. Nonviable biomass of biocontrol agent Papiliotrema flavescens OH 182.9 3C enhances growth of Fusarium graminearum and counteracts viable biomass reduction of Fusarium head blight[J]. Biological Control, 2019, 128: 48-55. DOI:10.1016/j.biocontrol.2018.09.006.