Share:


White mulberry (Morus alba L.) fruit-associated bacterial and fungal microbiota

    Juliana Lukša Affiliation
    ; Elena Servienė Affiliation

Abstract

Morus alba L. has been worldwide cultivated and commercially exploited plant with profound potential in environmental management, food and medicinal industries. Plant-associated microbial communities are playing an essential role in sustainable plant development. In the present study, the bacterial and fungal microorganism populations distributed on the white mulberry fruits harvested in the Czech Republic for the first time were characterized by metagenomics approach. A total of 62 bacterial and 37 fungal families were identified on white mulberry. Bacterial population was represented by the genera Tatumella, Leuconostoc, Frateuria and Pseudomonas, while fungal microorganisms – by Hanseniaspora, Cryptococcus, Cladosporium and Phoma. Both potentially beneficial, inducing resistance in the hosting plant, and pathogenic, responsible for disease development, microorganisms were detected. The information on the prevalence of bacterial and fungal microorganisms on the carposphere of M. alba is highly relevant for the development of strategies for environment-friendly plant cultivation, disease management and prevention.

Keyword : metagenomic analysis, Moraceae, fungal microbiota, bacterial microbiota

How to Cite
Lukša, J., & Servienė, E. (2020). White mulberry (Morus alba L.) fruit-associated bacterial and fungal microbiota. Journal of Environmental Engineering and Landscape Management, 28(4), 183-191. https://doi.org/10.3846/jeelm.2020.13735
Published in Issue
Nov 25, 2020
Abstract Views
158
PDF Downloads
111
SM_1 Downloads
31
SM_2 Downloads
18
Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

References

Aveskamp, M. M., De Gruyter, J., & Crous, P. W. (2008). Biology and recent developments in the systematics of Phoma, a complex genus of major quarantine significance. Fungal Diversity, 31, 1–18.

Bennett, A., Ponder, M., & Garcia-Diaz, J. (2018). Phoma infections: classification, potential food sources, and their clinical impact. Microorganisms, 6(3), 58. https://doi.org/10.3390/microorganisms6030058

Bernal-Martinez, L., Gomez-Lopez, A., Castelli, M. V., MesaArango, A. C., Zaragoza, O., Rodriguez-Tudela, J. L., & Cuenca-Estrella, M. (2010). Susceptibility profile of clinical isolates of non-Cryptococcus neoformans/non-Cryptococcus gattii Cryptococcus species and literature review. Medical Mycology, 48(1), 90–96. https://doi.org/10.3109/13693780902756073

Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Peña, A. G., Goodrich, J. K., Gordon, J. I., Huttley, G. A., Kelley, S. T., Knights, D., Koenig, J. E., Ley, R. E., Lozupone, C. A., McDonald, D., Muegge, B. D., Pirrung, M., Reeder, J., Sevinsky, J. R., Turnbaugh, P. J., Walters, W. A., Widmann, J., Yatsunenko, T., Zaneveld, J., & Knight, R. (2010). QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5), 335–336. https://doi.org/10.1038/nmeth.f.303

Chinnaswamy, K. P., & Harisprasad, K. B. (1995). Energy potentiality of mulberry. Indian Silk, 34(4), 15–18.

Cole, J. R., Wang, Q., Fish, J. A., Chai, B., McGarrell, D. M., Sun, Y., Brown, C. T., Porras-Alfaro, A., Kuske, C. R., & Tiedje, J. M. (2014). Ribosomal Database Project: Data and tools for high throughput rRNA analysis. Nucleic Acids Research, 42(D1), D633–D642. https://doi.org/10.1093/nar/gkt1244

Coutinho, T. A., & Venter, S. N. (2009). Pantoea ananatis: An unconventional plant pathogen. Molecular Plant Pathology, 10(3), 325–335. https://doi.org/10.1111/j.1364-3703.2009.00542.x

da Silva, A. M., Urban, R. C., Manfre, L. A., Brossard, M., & Moreira, M. Z. (2017). Soil quality attributes related to urbanization in Brazilian watershed. Journal of Environmental Engineering and Landscape Management, 25(4), 317–328. https://doi.org/10.3846/16486897.2017.1296451

Deveau, A., Bonito, G., Uehling, J., Paoletti, M., Becker, M., Bindschedler, S., Hacquard, S., Herve, V., Labbe, J., Lastovetsky, O., Mieszkin, S., Millet, L. J., Vanja, B., Junier, P., Bonfante, P., Krom, B., Olsson, S., van Elsas, J. D., & Wick, L. (2018). Bacterial – fungal interactions: Ecology, mechanisms and challenges. FEMS Microbiology Reviews, 42(3), 335–352. https://doi.org/10.1093/femsre/fuy008

Ercisli, S., & Orhan, E. (2007). Chemical composition of white (Morus alba), red (Morus rubra) and black (Morus nigra) mulberry fruits. Food Chemistry, 103(4), 1380–1384. https://doi.org/10.1016/j.foodchem.2006.10.054

Freimoser, F. M., Rueda-Mejia, M. P., Tilocca, B., & Migheli, Q. (2019). Biocontrol yeasts: Mechanisms and applications. World Journal of Microbiology and Biotechnology, 35, 154. https://doi.org/10.1007/s11274-019-2728-4

Graça, A., Santo, D., Esteves, E., Nunes, C., Abadias, M., & Quintas, C. (2015). Evaluation of microbial quality and yeast diversity in fresh-cut apple. Food Microbiology, 51, 179–185. https://doi.org/10.1016/j.fm.2015.06.003

Hashem, M., Alamri, S. A., Hesham, A. E. L., Al-Qahtani, F. M. H., & Kilany, M. (2014). Biocontrol of apple blue mould by new yeast strains: Cryptococcus albidus KKUY0017 and Wickerhamomyces anomalus KKUY0051 and their mode of action. Biocontrol Science and Technology, 24(10), 1137– 1152. https://doi.org/10.1080/09583157.2014.926857

Holland, R., & Liu, S.-Q. (2011). Lactic Acid Bacteria | Leuconostoc spp. In Encyclopedia of dairy sciences (pp. 138–142). Elsevier. https://doi.org/10.1016/B978-0-12-374407-4.00267-3

Jiang, Y., Huang, R., Yan, X., Jia, C., Jiang, S., & Long, T. (2017). Mulberry for environmental protection. Pakistan Journal of Botany, 49(2), 781–788.

Kõljalg, U., Nilsson, R. H., Abarenkov, K., Tedersoo, L., Taylor, A. F. S., Bahram, M., Bates, S. T., Bruns, T. D., Bengtsson-Palme, J., Callaghan, T. M., Douglas, B., Drenkhan, T., Eberhardt, U., Dueñas, M., Grebenc, T., Griffith, G. W., Hartmann, M., Kirk, P. M., Kohout, P., Larsson, E., Lindahl, B. D., Lücking, R., Martín, M. P., Matheny, P. B., Nguyen, N. H., Niskanen, T., Oja, J., Peay, K. G., Peintner, U., Peterson, M., Põldmaa, K., Saag, L., Saar, I., Schüßler, A., Scott, J. A., Senés, C., Smith, M. E., Suija, A., Taylor, D. L., Telleria, M. T., Weiss, M., & Larsson, K.-H. (2013). Towards a unified paradigm for sequence-based identification of fungi. Molecular Ecology, 22(21), 5271–5277. https://doi.org/10.1111/mec.12481

Khoshdel, A., & Vaziri, B. M. (2016). Novel mathematical models for prediction of microbial growth kinetics and contaminant degradation in bioremediation process. Journal of Environmental Engineering and Landscape Management, 24(3), 157– 164. https://doi.org/10.3846/16486897.2016.1142446

Li, W., Fu, L., Niu, B., Wu, S., & Wooley, J. (2012). Ultrafast clustering algorithms for metagenomic sequence analysis. Briefings in Bioinformatics, 13(6), 656–668. https://doi.org/10.1093/bib/bbs035

Lidor, O., Santos-Garcia, D., Mozes-Daube, N., Naor, V., Cohen, E., Iasur-Kruh, L., Bahar, O., & Zchori-Fein, E. (2019). Frateuria defendens sp. nov., bacterium isolated from the yellows grapevine’s disease vector Hyalesthes obsoletus. International Journal of Systematic and Evolutionary Microbiology, 69(5), 1281–1287. https://doi.org/10.1099/ijsem.0.003305

Ligon, J. M., Hill, D. S., Hammer, P. E., Torkewitz, N. R., Hofmann, D., Kempf, H.-J., & Pee, K.-H. van. (2000). Natural products with antifungal activity from Pseudomonas biocontrol bacteria. Pest Management Science, 56(8), 688–695. https://doi.org/10.1002/1526-4998(200008)56:8<688::AIDPS186>3.0.CO;2-V

Lindow, S. E., & Brandl, M. T. (2003). Microbiology of the phyllosphere. Applied and Environmental Microbiology, 69(4), 1875–1883. https://doi.org/10.1128/AEM.69.4.1875-1883.2003

Liu, H. M., Guo, J. H., Cheng, Y. J., Luo, L., Liu, P., Wang, B. Q., Deng, B. X., & Long, C. A. (2010). Control of gray mold of grape by Hanseniaspora uvarum and its effects on postharvest quality parameters. Annals of Microbiology, 60(1), 31–35. https://doi.org/10.1007/s13213-010-0018-3

Liu, J., Sui, Y., Wisniewski, M., Droby, S., & Liu, Y. (2013). Review: Utilization of antagonistic yeasts to manage postharvest fungal diseases of fruit. International Journal of Food Microbiology, 167(2), 153–160. https://doi.org/10.1016/j.ijfoodmicro.2013.09.004

Łochyńska, M. (2015). Energy and nutritional properties of the white mulberry (Morus alba L.). Journal of Agricultural Science and Technology A, 5(9). https://doi.org/10.17265/2161-6256/2015.09.001

Lukša, J., Vepštaitė-Monstavičė, I., Yurchenko, V., Serva, S., & Servienė, E. (2018). High content analysis of sea buckthorn, black chokeberry, red and white currants microbiota – A pilot study. Food Research International, 111, 597–606. https://doi.org/10.1016/j.foodres.2018.05.060

Magoč, T., & Salzberg, S. L. (2011). FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics (Oxford, England), 27(21), 2957–2963. https://doi.org/10.1093/bioinformatics/btr507

Mahboubi, M. (2019). Morus alba (mulberry), a natural potent compound in management of obesity. Pharmacological Research, 146, 104341. https://doi.org/10.1016/j.phrs.2019.104341

Mardaneh, J., Soltan Dallal, M. M., Taheripoor, M., & Rajabi, Z. (2014). Isolation, identification and antimicrobial susceptibility pattern of Tatumella ptyseos strains isolated from powdered infant formula milk consumed in neonatal intensive care unit: first report from Iran. Jundishapur Journal of Microbiology, 7(6), e10608. https://doi.org/10.5812/jjm.10608

Oliveira, R. C., Goncalves, S. S., Oliveira, M. S., Dilkin, P., Mallmann, C. A., Freitas, R. S., Bianchi, P., & Correa, B. (2017). Natural occurrence of tenuazonic acid and Phoma sorghina in Brazilian sorghum grains at different maturity stages. Food Chemistry, 230, 491–496. https://doi.org/10.1016/j.foodchem.2017.03.079

Ondov, B. D., Bergman, N. H., & Phillippy, A. M. (2011). Interactive metagenomic visualization in a Web browser. BMC Bioinformatics, 12(1), 385. https://doi.org/10.1186/1471-2105-12-385

Ou, T., Xu, W., Wang, F., Strobel, G., Zhou, Z., Xiang, Z., Liu, J., & Xie, J. (2019). A microbiome study reveals seasonal variation in endophytic bacteria among different mulberry cultivars. Computational and Structural Biotechnology Journal, 17, 1091–1100. https://doi.org/10.1016/j.csbj.2019.07.018

Pinto, C., Pinho, D., Cardoso, R., Custódio, V., Fernandes, J., Sousa, S., Pinheiro M., Egas, C., & Gomes, A. C. (2015). Wine fermentation microbiome: A landscape from different Portuguese wine appellations. Frontiers in Microbiology, 6, 905. https://doi.org/10.3389/fmicb.2015.00905

Rodrigues, E. L., Marcelino, G., Silva, G. T., Figueiredo, P. S., Garcez, W. S., Corsino, J., Guimarães, R. de C. A., & Freitas, K. de C. (2019). Nutraceutical and medicinal potential of the Morus species in metabolic dysfunctions. International Journal of Molecular Sciences, 20(2), 301. https://doi.org/10.3390/ijms20020301

Sandoval-Denis, M., Gené, J., Sutton, D. A., Wiederhold, N. P., Cano-Lira, J. F., & Guarro, J. (2016). New species of Cladosporium associated with human and animal infections. Persoonia – Molecular Phylogeny and Evolution of Fungi, 36(1), 281–298. https://doi.org/10.3767/003158516X691951

Shin, S.-Y., & Han, N. S. (2015). Leuconostoc spp. as starters and their beneficial roles in fermented foods. In M. T. Liong (Ed.), Beneficial Microorganisms in food and nutraceuticals. Microbiology monographs (Vol. 27, pp. 111–132). Springer, Cham. https://doi.org/10.1007/978-3-319-23177-8_5

Termorshuizen, A. J. (2007). Fungal and fungus-like pathogens of potato. In Potato biology and biotechnology (pp. 643–665). Elsevier. https://doi.org/10.1016/B978-044451018-1/50071-3

Tilocca, B., Cao, A., & Migheli, Q. (2020). Scent of a Killer: Microbial volatilome and its role in the biological control of plant pathogens. Frontiers in Microbiology, 11, 1–13. https://doi.org/10.3389/fmicb.2020.00041

Trotel-Aziz, P., Couderchet, M., Biagianti, S., & Aziz, A. (2008). Characterization of new bacterial biocontrol agents Acinetobacter, Bacillus, Pantoea and Pseudomonas spp. mediating grapevine resistance against Botrytis cinerea. Environmental and Experimental Botany, 64(1), 21–32. https://doi.org/10.1016/j.envexpbot.2007.12.009

Vadkertiová, R., Molnárová, J., Vránová, D., & Sláviková, E. (2012). Yeasts and yeast-like organisms associated with fruits and blossoms of different fruit trees. Canadian Journal of Microbiology, 58(12), 1344–1352. https://doi.org/10.1139/cjm-2012-0468

Vepštaitė-Monstavičė, I., Lukša, J., Stanevičienė, R., StrazdaitėŽielienė, Ž., Yurchenko, V., Serva, S., & Servienė, E. (2018). Distribution of apple and blackcurrant microbiota in Lithuania and the Czech Republic. Microbiological Research, 206, 1–8. https://doi.org/10.1016/j.micres.2017.09.004

Wang, X., Radwan, M. M., Taráwneh, A. H., Gao, J., Wedge, D. E., Rosa, L. H., Cutler, H. G., & Cutler, S. J. (2013). Antifungal activity against plant pathogens of metabolites from the endophytic fungus cladosporium cladosporioides. Journal of Agricultural and Food Chemistry, 61(19), 4551–4555. https://doi.org/10.1021/jf400212y

Xu, W., Wang, F., Zhang, M., Ou, T., Wang, R., Strobel, G., Xiang, Z., Zhou, Z., & Xie, J. (2019). Diversity of cultivable endophytic bacteria in mulberry and their potential for antimicrobial and plant growth-promoting activities. Microbiological Research, 229, 126328. https://doi.org/10.1016/j.micres.2019.126328

Yu, C., Hu, X., Deng, W., Li, Y., Han, G., & Ye, C. (2016). Soil fungal community comparison of different mulberry genotypes and the relationship with mulberry fruit sclerotiniosis. Scientific Reports, 6(1), 28365. https://doi.org/10.1038/srep28365

Zhang, H., Ma, Z., Luo, X., & Li, X. (2018). Effects of mulberry fruit (Morus alba L.) consumption on health outcomes: A mini-review. Antioxidants, 7(5), 69. https://doi.org/10.3390/antiox7050069

Zhang, M. M., Wang, N., Zhang, J., Hu, Y., Cai, D., Guo, J., Wu, D., & Sun, G. (2019). Soil physicochemical properties and the rhizosphere soil fungal community in a mulberry (Morus alba L.)/Alfalfa (Medicago sativa L.) intercropping system. Forests, 10(2), 167. https://doi.org/10.3390/f10020167