Endophytic Bacteria are Potential Source of Medicinal Plant Therapeutics and Bioactive Compound Synthesis
Tanwy Chowdhury1, Md. Asaduzzaman Shishir2, Md. Fakruddin1*
Australian Herbal Insight 7(1) 1-8 https://doi.org/10.25163/ahi.719985
Submitted: 01 April 2024 Revised: 07 June 2024 Published: 09 June 2024
This review discusses endophytic bacteria, which is a novel, large source of bioactive compounds that enhance plant therapeutics and advance drug discovery potential.
Abstract
Background: Endophytic bacteria residing within plant tissues play a crucial role in promoting plant health and enhancing the production of secondary metabolites, thereby increasing the therapeutic value of medicinal plants. These bacteria exhibit significant taxonomic diversity and ecological distribution, forming symbiotic relationships with their host plants, ranging from mutualism to commensalism. Methods: This review discusses the ecological niches, diversity, and interactions of endophytic bacteria within various medicinal plants. Sampling of roots, stems, leaves, and other plant tissues was conducted, followed by isolation and identification of bacterial species using molecular techniques. The relationships between endophytic bacteria and their hosts were analyzed through ecological assessments and bioactivity assays. Results: Endophytic bacteria demonstrated substantial diversity, predominantly belonging to phyla such as Proteobacteria, Actinobacteria, and Firmicutes. Notable genera included Bacillus, Pseudomonas, and Streptomyces, which exhibited plant growth-promoting and antimicrobial properties. The study identified specific endophytes that enhanced the production of key bioactive compounds in medicinal plants, contributing to their therapeutic efficacy. Conclusion: The symbiotic relationships between endophytic bacteria and medicinal plants reveal a largely untapped reservoir of bioactive compounds with promising therapeutic applications. Understanding the ecological dynamics and biochemical pathways involved in these interactions offers opportunities for innovative approaches in drug discovery and sustainable agriculture. Future research should focus on characterizing these microbial communities and their metabolites to unlock their full potential in medicine and beyond.
Keywords: Endophytic bacteria, phytosymbionts, medicinal plants, bioactive compounds, drug discovery, secondary metabolites, antimicrobial agents, plant-microbe interactions, bioprospecting, pharmaceutical potential.
References
Afzal, I., Shinwari, Z. K., Sikandar, S., & Shahzad, S. (2019). Plant beneficial endophytic bacteria: Mechanisms, diversity, host range and genetic determinants. Microbiological Research, 221, 36–49. https://doi.org/10.1016/j.micres.2019.02.001
Alvin, A., Miller, K. I., & Neilan, B. A. (2014). Exploring the potential of endophytes from medicinal plants as sources of antimycobacterial compounds. Microbiological Research, 169(7–8), 483–495. https://doi.org/10.1016/j.micres.2013.12.009
Anand, U., Pal, T., Yadav, N., Singh, V. K., Tripathi, V., Choudhary, K. K., Shukla, A. K., Sunita, K., Kumar, A., Bontempi, E., Ma, Y., Kolton, M., & Singh, A. K. (2023). Current Scenario and Future Prospects of Endophytic Microbes: Promising Candidates for Abiotic and Biotic Stress Management for Agricultural and Environmental Sustainability. Microbial Ecology, 86(3), 1455–1486. https://doi.org/10.1007/s00248-023-02190-1
Blin, K., Wolf, T., Chevrette, M. G., Lu, X., Schwalen, C. J., Kautsar, S. A., Suarez Duran, H. G., de los Santos, E. L. C., Kim, H. U., Nave, M., Dickschat, J. S., Mitchell, D. A., Shelest, E., Breitling, R., Takano, E., Lee, S. Y., Weber, T., & Medema, M. H. (2017). antiSMASH 4.0—Improvements in chemistry prediction and gene cluster boundary identification. Nucleic Acids Research, 45(W1), W36–W41. https://doi.org/10.1093/nar/gkx319
Brader, G., Compant, S., Vescio, K., Mitter, B., Trognitz, F., Ma, L.-J., & Sessitsch, A. (2017). Ecology and Genomic Insights into Plant-Pathogenic and Plant-Nonpathogenic Endophytes. Annual Review of Phytopathology, 55(1), 61–83. https://doi.org/10.1146/annurev-phyto-080516-035641
Castillo, U. F., Strobel, G. A., Ford, E. J., Hess, W. M., Porter, H., Jensen, J. B., Albert, H., Robison, R., Condron, M. A. M., Teplow, D. B., Stevens, D., & Yaver, D. (2002). Munumbicins, wide-spectrum antibiotics produced by Streptomyces NRRL 30562, endophytic on Kennedia nigriscans a aThe GenBank accession number for the sequence determined in this work is AY127079. Microbiology, 148(9), 2675–2685. https://doi.org/10.1099/00221287-148-9-2675
Christinaki, A. C., Myridakis, A. I., & Kouvelis, V. N. (2024). Genomic insights into the evolution and adaptation of secondary metabolite gene clusters in fungicolous species Cladobotryum mycophilum ATHUM6906. G3 (Bethesda, Md.), 14(4), jkae006. https://doi.org/10.1093/g3journal/jkae006
Covington, B. C., McLean, J. A., & Bachmann, B. O. (2017). Comparative mass spectrometry-based metabolomics strategies for the investigation of microbial secondary metabolites. Natural Product Reports, 34(1), 6–24. https://doi.org/10.1039/C6NP00048G
de Oliveira Costa, L. E., de Queiroz, M. V., Borges, A. C., de Moraes, C. A., & de Araújo, E. F. (2012). Isolation and characterization of endophytic bacteria isolated from the leaves of the common bean (Phaseolus vulgaris). Brazilian Journal of Microbiology: [Publication of the Brazilian Society for Microbiology], 43(4), 1562–1575. https://doi.org/10.1590/S1517-838220120004000041
Dias, D. A., Urban, S., & Roessner, U. (2012). A Historical Overview of Natural Products in Drug Discovery. Metabolites, 2(2), 303–336. https://doi.org/10.3390/metabo2020303
Digra, S., & Nonzom, S. (2023). An insight into endophytic antimicrobial compounds: An updated analysis. Plant Biotechnology Reports, 1–31. https://doi.org/10.1007/s11816-023-00824-x
Djuuna, I. A. F., Prabawardani, S., & Massora, M. (2022). Population Distribution of Phosphate-solubilizing Microorganisms in Agricultural Soil. Microbes and Environments, 37(1), n/a. https://doi.org/10.1264/jsme2.ME21041
Eberl, F., Uhe, C., & Unsicker, S. B. (2019). Friend or foe? The role of leaf-inhabiting fungal pathogens and endophytes in tree-insect interactions. Fungal Ecology, 38, 104–112. https://doi.org/10.1016/j.funeco.2018.04.003
Eid, A. M., Fouda, A., Abdel-Rahman, M. A., Salem, S. S., Elsaied, A., Oelmüller, R., Hijri, M., Bhowmik, A., Elkelish, A., & Hassan, S. E.-D. (2021). Harnessing Bacterial Endophytes for Promotion of Plant Growth and Biotechnological Applications: An Overview. Plants (Basel, Switzerland), 10(5), 935. https://doi.org/10.3390/plants10050935
Eisenhut, M., Pick, T. R., Bordych, C., & Weber, A. P. M. (2013). Towards closing the remaining gaps in photorespiration – the essential but unexplored role of transport proteins. Plant Biology, 15(4), 676–685. https://doi.org/10.1111/j.1438-8677.2012.00690.x
El-Shafey, N. M., Marzouk, M. A., Yasser, M. M., Shaban, S. A., Beemster, G. T. S., & AbdElgawad, H. (2021). Harnessing Endophytic Fungi for Enhancing Growth, Tolerance and Quality of Rose-Scented Geranium (Pelargonium graveolens (L’Hér) Thunb.) Plants under Cadmium Stress: A Biochemical Study. Journal of Fungi (Basel, Switzerland), 7(12), 1039. https://doi.org/10.3390/jof7121039
Fazeli, M. (2024). The Endophytes: A New Resource for Vulnerable Plant Bioactive Compounds. In M. Santana De Oliveira, E. Helena De Aguiar Andrade, R. Kumar, & S. N. Mali (Eds.), Medicinal Plants—Chemical, Biochemical, and Pharmacological Approaches. IntechOpen. https://doi.org/10.5772/intechopen.112931
Gakuubi, M. M., Munusamy, M., Liang, Z.-X., & Ng, S. B. (2021). Fungal Endophytes: A Promising Frontier for Discovery of Novel Bioactive Compounds. Journal of Fungi (Basel, Switzerland), 7(10), 786. https://doi.org/10.3390/jof7100786
Gazis, R., Skaltsas, D., & Chaverri, P. (2014). Novel endophytic lineages of Tolypocladium provide new insights into the ecology and evolution of Cordyceps -like fungi. Mycologia, 106(6), 1090–1105. https://doi.org/10.3852/13-346
Glick, B. R., & Gamalero, E. (2021). Recent Developments in the Study of Plant Microbiomes. Microorganisms, 9(7), 1533. https://doi.org/10.3390/microorganisms9071533
Goggin, F. L. (2007). Plant–aphid interactions: Molecular and ecological perspectives. Current Opinion in Plant Biology, 10(4), 399–408. https://doi.org/10.1016/j.pbi.2007.06.004
Gouda, S., Das, G., Sen, S. K., Shin, H.-S., & Patra, J. K. (2016). Endophytes: A Treasure House of Bioactive Compounds of Medicinal Importance. Frontiers in Microbiology, 7, 1538. https://doi.org/10.3389/fmicb.2016.01538
Guha, T., & Mandal Biswas, S. (2024). Recent progress in the role of seed endophytic bacteria as plant growth-promoting microorganisms and biocontrol agents. World Journal of Microbiology and Biotechnology, 40(7), 218. https://doi.org/10.1007/s11274-024-04031-w
Guo, B., Wang, Y., Sun, X., & Tang, K. (2008). Bioactive natural products from endophytes: A review. Applied Biochemistry and Microbiology, 44(2), 136–142. https://doi.org/10.1134/S0003683808020026
Gupta, S., Chaturvedi, P., Kulkarni, M. G., & Van Staden, J. (2020). A critical review on exploiting the pharmaceutical potential of plant endophytic fungi. Biotechnology Advances, 39, 107462. https://doi.org/10.1016/j.biotechadv.2019.107462
Hardoim, P. R., Van Overbeek, L. S., Berg, G., Pirttilä, A. M., Compant, S., Campisano, A., Döring, M., & Sessitsch, A. (2015). The Hidden World within Plants: Ecological and Evolutionary Considerations for Defining Functioning of Microbial Endophytes. Microbiology and Molecular Biology Reviews, 79(3), 293–320. https://doi.org/10.1128/MMBR.00050-14
Hardoim, P. R., Van Overbeek, L. S., & Elsas, J. D. V. (2008). Properties of bacterial endophytes and their proposed role in plant growth. Trends in Microbiology, 16(10), 463–471. https://doi.org/10.1016/j.tim.2008.07.008
Hashem, A. H., Attia, M. S., Kandil, E. K., Fawzi, M. M., Abdelrahman, A. S., Khader, M. S., Khodaira, M. A., Emam, A. E., Goma, M. A., & Abdelaziz, A. M. (2023). Correction to: Bioactive compounds and biomedical applications of endophytic fungi: a recent review. Microbial Cell Factories, 22(1), 122. https://doi.org/10.1186/s12934-023-02131-0
Hu, Y., Wei Gy, G., Wen, J., Chang, L., Chen, Y., Wang, Y., & Nizamani, M. (2024). Endophytic fungi: Tracing the evolutionary roots and exploring the diversity of plant-fungal symbioses. Current Research in Environmental & Applied Mycology, 14(1), 1–48. https://doi.org/10.5943/cream/14/1/1
Jia, M., Chen, L., Xin, H.-L., Zheng, C.-J., Rahman, K., Han, T., & Qin, L.-P. (2016). A Friendly Relationship between Endophytic Fungi and Medicinal Plants: A Systematic Review. Frontiers in Microbiology, 7. https://doi.org/10.3389/fmicb.2016.00906
Jiang, S., Chen, Y., Han, S., Lv, L., & Li, L. (2022). Next-Generation Sequencing Applications for the Study of Fungal Pathogens. Microorganisms, 10(10), 1882. https://doi.org/10.3390/microorganisms10101882
Johnston-Monje, D., Castillo-Avila, D. K., Raizada, M. N., & Becerra Lopez-Lavalle, L. A. (2019). Paying the Rent: How Endophytic Microorganisms Help Plant Hosts Obtain Nutrients. In Comprehensive Biotechnology (pp. 770–788). Elsevier. https://doi.org/10.1016/B978-0-444-64046-8.00253-6
Kamat, S., Kumari, M., Sajna, K. V., Shruthi Mohan, & Jayabaskaran, C. (2022). Marine endophytes from the Indian coasts: The untapped sources of sustainable anticancer drug discovery. Sustainable Chemistry and Pharmacy, 27, 100675. https://doi.org/10.1016/j.scp.2022.100675
Kousar, R., Naeem, M., Jamaludin, M. I., Arshad, A., Shamsuri, A. N., Ansari, N., Akhtar, S., Hazafa, A., Uddin, J., Khan, A., & Al-Harrasi, A. (2022). Exploring the anticancer activities of novel bioactive compounds derived from endophytic fungi: Mechanisms of action, current challenges and future perspectives. American Journal of Cancer Research, 12(7), 2897–2919.
Krabel, D., Morgenstern, K., & Herzog, S. (2013). Endophytes in changing environments—Do we need new concepts in forest management? iForest - Biogeosciences and Forestry, 6(3), 109–112. https://doi.org/10.3832/ifor0932-006
Loeven, N. A., Medici, N. P., & Bliska, J. B. (2020). The pyrin inflammasome in host–microbe interactions. Current Opinion in Microbiology, 54, 77–86. https://doi.org/10.1016/j.mib.2020.01.005
Madasi, A., Ajmeera, A., Renuka, G., Vemireddy, B., & Vanteru, K. R. (2021). Production of Extracellular Enzymes, Antimicrobial and other Agriculturally Important Metabolites by Fungal Endophytes of Litsea glutinosa (Lour.) C.B.Rob. A Medicinal Plant. Journal of Pure and Applied Microbiology, 15(4), 2317–2328. https://doi.org/10.22207/JPAM.15.4.56
Maiden, M. C. J., Bygraves, J. A., Feil, E., Morelli, G., Russell, J. E., Urwin, R., Zhang, Q., Zhou, J., Zurth, K., Caugant, D. A., Feavers, I. M., Achtman, M., & Spratt, B. G. (1998). Multilocus sequence typing: A portable approach to the identification of clones within populations of pathogenic microorganisms. Proceedings of the National Academy of Sciences, 95(6), 3140–3145. https://doi.org/10.1073/pnas.95.6.3140
Manganyi, M. C., & Ateba, C. N. (2020). Untapped Potentials of Endophytic Fungi: A Review of Novel Bioactive Compounds with Biological Applications. Microorganisms, 8(12), 1934. https://doi.org/10.3390/microorganisms8121934
Marchut-Mikolajczyk, O., Chlebicz, M., Kawecka, M., Michalak, A., Prucnal, F., Nielipinski, M., Filipek, J., Jankowska, M., Perek, Z., Drozdzynski, P., Rutkowska, N., & Otlewska, A. (2023). Endophytic bacteria isolated from Urtica dioica L.- preliminary screening for enzyme and polyphenols production. Microbial Cell Factories, 22(1), 169. https://doi.org/10.1186/s12934-023-02167-2
Matsumoto, A., & Takahashi, Y. (2017). Endophytic actinomycetes: Promising source of novel bioactive compounds. The Journal of Antibiotics, 70(5), 514–519. https://doi.org/10.1038/ja.2017.20
Medison, R. G., Tan, L., Medison, M. B., & Chiwina, K. E. (2022). Use of beneficial bacterial endophytes: A practical strategy to achieve sustainable agriculture. AIMS Microbiology, 8(4), 624–643. https://doi.org/10.3934/microbiol.2022040
Moussa, A. Y. (2024). Endophytes: A uniquely tailored source of potential antibiotic adjuvants. Archives of Microbiology, 206(5), 207. https://doi.org/10.1007/s00203-024-03891-y
Muthu Narayanan, M., Ahmad, N., Shivanand, P., & Metali, F. (2022). The Role of Endophytes in Combating Fungal- and Bacterial-Induced Stress in Plants. Molecules (Basel, Switzerland), 27(19), 6549. https://doi.org/10.3390/molecules27196549
Naughton, L. M., Romano, S., O’Gara, F., & Dobson, A. D. W. (2017). Identification of Secondary Metabolite Gene Clusters in the Pseudovibrio Genus Reveals Encouraging Biosynthetic Potential toward the Production of Novel Bioactive Compounds. Frontiers in Microbiology, 8, 1494. https://doi.org/10.3389/fmicb.2017.01494
Ongena, M., & Jacques, P. (2008). Bacillus lipopeptides: Versatile weapons for plant disease biocontrol. Trends in Microbiology, 16(3), 115–125. https://doi.org/10.1016/j.tim.2007.12.009
Pimentel, M. R., Molina, G., Dionísio, A. P., Maróstica Junior, M. R., & Pastore, G. M. (2011). The Use of Endophytes to Obtain Bioactive Compounds and Their Application in Biotransformation Process. Biotechnology Research International, 2011, 1–11. https://doi.org/10.4061/2011/576286
Rai, N., Kumari Keshri, P., Verma, A., Kamble, S. C., Mishra, P., Barik, S., Kumar Singh, S., & Gautam, V. (2021). Plant associated fungal endophytes as a source of natural bioactive compounds. Mycology, 12(3), 139–159. https://doi.org/10.1080/21501203.2020.1870579
Renugadevi, R., Ayyappadas, M. P., Priya, V. S., Shobana, M. F., & Vivekanandhan, K. (2021). Applications of bacterial endophytes and their advanced identification methodologies. Journal of Applied Biology & Biotechnology. https://doi.org/10.7324/JABB.2021.9606
Ríos, J. L., & Recio, M. C. (2005). Medicinal plants and antimicrobial activity. Journal of Ethnopharmacology, 100(1–2), 80–84. https://doi.org/10.1016/j.jep.2005.04.025
Rosenblueth, M., & Martínez-Romero, E. (2006). Bacterial Endophytes and Their Interactions with Hosts. Molecular Plant-Microbe Interactions®, 19(8), 827–837. https://doi.org/10.1094/MPMI-19-0827
Ryan, R. P., Germaine, K., Franks, A., Ryan, D. J., & Dowling, D. N. (2008). Bacterial endophytes: Recent developments and applications. FEMS Microbiology Letters, 278(1), 1–9. https://doi.org/10.1111/j.1574-6968.2007.00918.x
Salvi, P., Mahawar, H., Agarrwal, R., Kajal, null, Gautam, V., & Deshmukh, R. (2022). Advancement in the molecular perspective of plant-endophytic interaction to mitigate drought stress in plants. Frontiers in Microbiology, 13, 981355. https://doi.org/10.3389/fmicb.2022.981355
Santoyo, G., Moreno-Hagelsieb, G., Del Carmen Orozco-Mosqueda, Ma., & Glick, B. R. (2016). Plant growth-promoting bacterial endophytes. Microbiological Research, 183, 92–99. https://doi.org/10.1016/j.micres.2015.11.008
Selim, K. (2012). Biology of Endophytic Fungi. Current Research in Environmental & Applied Mycology, 2(1), 31–82. https://doi.org/10.5943/cream/2/1/3
Sessitsch, A., Reiter, B., Pfeifer, U., & Wilhelm, E. (2002). Cultivation-independent population analysis of bacterial endophytes in three potato varieties based on eubacterial and Actinomycetes-specific PCR of 16S rRNA genes. FEMS Microbiology Ecology, 39(1), 23–32. https://doi.org/10.1111/j.1574-6941.2002.tb00903.x
Shaffique, S., Khan, M. A., Wani, S. H., Pande, A., Imran, M., Kang, S.-M., Rahim, W., Khan, S. A., Bhatta, D., Kwon, E.-H., & Lee, I.-J. (2022). A Review on the Role of Endophytes and Plant Growth Promoting Rhizobacteria in Mitigating Heat Stress in Plants. Microorganisms, 10(7), 1286. https://doi.org/10.3390/microorganisms10071286
Singh, A., Singh, D. K., Kharwar, R. N., White, J. F., & Gond, S. K. (2021). Fungal Endophytes as Efficient Sources of Plant-Derived Bioactive Compounds and Their Prospective Applications in Natural Product Drug Discovery: Insights, Avenues, and Challenges. Microorganisms, 9(1), 197. https://doi.org/10.3390/microorganisms9010197
Singh, M., Kumar, A., Singh, R., & Pandey, K. D. (2017). Endophytic bacteria: A new source of bioactive compounds. 3 Biotech, 7(5), 315. https://doi.org/10.1007/s13205-017-0942-z
Singh, N. A., & Jain, R. (2022). Diversity and Bioactive Potential of Endophytic Bacteria from High-Value Medicinal Plants. In A. K. Singh, V. Tripathi, A. K. Shukla, & P. Kumar (Eds.), Bacterial Endophytes for Sustainable Agriculture and Environmental Management (pp. 45–69). Springer Singapore. https://doi.org/10.1007/978-981-16-4497-9_3
Smith, C. A., Maille, G. O., Want, E. J., Qin, C., Trauger, S. A., Brandon, T. R., Custodio, D. E., Abagyan, R., & Siuzdak, G. (2005). METLIN: A Metabolite Mass Spectral Database. Therapeutic Drug Monitoring, 27(6), 747–751. https://doi.org/10.1097/01.ftd.0000179845.53213.39
Stierle, A., Strobel, G., & Stierle, D. (1993). Taxol and Taxane Production by Taxomyces andreanae , an Endophytic Fungus of Pacific Yew. Science, 260(5105), 214–216. https://doi.org/10.1126/science.8097061
Strobel, G. (2018). The Emergence of Endophytic Microbes and Their Biological Promise. Journal of Fungi, 4(2), 57. https://doi.org/10.3390/jof4020057
Strobel, G., & Daisy, B. (2003). Bioprospecting for microbial endophytes and their natural products. Microbiology and Molecular Biology Reviews: MMBR, 67(4), 491–502. https://doi.org/10.1128/MMBR.67.4.491-502.2003
Strobel, G., Daisy, B., Castillo, U., & Harper, J. (2004). Natural Products from Endophytic Microorganisms. Journal of Natural Products, 67(2), 257–268. https://doi.org/10.1021/np030397v
Tiwari, P., & Bae, H. (2020). Horizontal Gene Transfer and Endophytes: An Implication for the Acquisition of Novel Traits. Plants, 9(3), 305. https://doi.org/10.3390/plants9030305
Tshikhudo, P. P., Ntushelo, K., & Mudau, F. N. (2023). Sustainable Applications of Endophytic Bacteria and Their Physiological/Biochemical Roles on Medicinal and Herbal Plants: Review. Microorganisms, 11(2), 453. https://doi.org/10.3390/microorganisms11020453
Tsipinana, S., Husseiny, S., Alayande, K. A., Raslan, M., Amoo, S., & Adeleke, R. (2023). Contribution of endophytes towards improving plant bioactive metabolites: A rescue option against red-taping of medicinal plants. Frontiers in Plant Science, 14, 1248319. https://doi.org/10.3389/fpls.2023.1248319
Uzma, F., Mohan, C. D., Hashem, A., Konappa, N. M., Rangappa, S., Kamath, P. V., Singh, B. P., Mudili, V., Gupta, V. K., Siddaiah, C. N., Chowdappa, S., Alqarawi, A. A., & Abd Allah, E. F. (2018). Endophytic Fungi-Alternative Sources of Cytotoxic Compounds: A Review. Frontiers in Pharmacology, 9, 309. https://doi.org/10.3389/fphar.2018.00309
Verma, V. C., Kharwar, R. N., & Strobel, G. A. (2009). Chemical and functional diversity of natural products from plant associated endophytic fungi. Natural Product Communications, 4(11), 1511–1532.
Watts, D., Palombo, E. A., Jaimes Castillo, A., & Zaferanloo, B. (2023). Endophytes in Agriculture: Potential to Improve Yields and Tolerances of Agricultural Crops. Microorganisms, 11(5), 1276. https://doi.org/10.3390/microorganisms11051276
Wu, W., Chen, W., Liu, S., Wu, J., Zhu, Y., Qin, L., & Zhu, B. (2021). Beneficial Relationships Between Endophytic Bacteria and Medicinal Plants. Frontiers in Plant Science, 12, 646146. https://doi.org/10.3389/fpls.2021.646146
Xia, Y., Liu, J., Chen, C., Mo, X., Tan, Q., He, Y., Wang, Z., Yin, J., & Zhou, G. (2022). The Multifunctions and Future Prospects of Endophytes and Their Metabolites in Plant Disease Management. Microorganisms, 10(5), 1072. https://doi.org/10.3390/microorganisms10051072
Zanne, A. E., Abarenkov, K., Afkhami, M. E., Aguilar-Trigueros, C. A., Bates, S., Bhatnagar, J. M., Busby, P. E., Christian, N., Cornwell, W. K., Crowther, T. W., Flores-Moreno, H., Floudas, D., Gazis, R., Hibbett, D., Kennedy, P., Lindner, D. L., Maynard, D. S., Milo, A. M., Nilsson, R. H., … Treseder, K. K. (2020). Fungal functional ecology: Bringing a trait-based approach to plant-associated fungi. Biological Reviews, 95(2), 409–433. https://doi.org/10.1111/brv.12570
Zhuo, M., An, T., Zhang, C., & Wang, Z. (2020). Characterization of Microbiota in Cancerous Lung and the Contralateral Non-Cancerous Lung Within Lung Cancer Patients. Frontiers in Oncology, 10, 1584. https://doi.org/10.3389/fonc.2020.01584
Zimmerman, N. B., & Vitousek, P. M. (2012). Fungal endophyte communities reflect environmental structuring across a Hawaiian landscape. Proceedings of the National Academy of Sciences, 109(32), 13022–13027. https://doi.org/10.1073/pnas.1209872109
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