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DOI: 10.1055/a-2420-0270
Medicinal Plant Microbiomes: Factors Affecting Bacterial and Fungal Community Composition
Supported by: National Center for Complementary and Integrative Health P50 AT0000155Supported by: National Center for Complementary and Integrative Health T32 AT007533
Abstract
This exploratory study was designed to identify factors implicating microbial influence on medicinal plant metabolomes. Utilizing a whole-microbiome approach, amplicon sequencing was used to identify the makeup of fungal and bacterial assemblages from endophytic (interior) and epiphytic (external) environments in two different sets of congeneric host-plant pairs, with collection of multiple samples of two medicinal plant species (Actaea racemosa, Rhodiola rosea) and two generic analogs (Actaea rubra, Rhodiola integrifolia). Diversity analysis of microbial assemblages revealed the influence of three primary factors driving variance in microbial community composition: host-plant taxonomy, the compartmentalization of microbial communities within discrete plant parts, and the scale of distance (microhabitat heterogeneity) between sampling locations. These three factors accounted for ~ 60% of variance within and between investigated microbiomes. Across all our collections, bacterial populations were more diverse than fungi (per compartment), and microbial density in epiphytic compartments (aerial parts, rhizosphere) were higher than those of endophytes (leaf and root). These comparative data point to key loci associated with variation between congeneric pairs and plant genera, providing insight into the complex and contrasting relationships found within this multi-kingdom coevolutionary relationship. Although reflective of only a limited set of botanical source materials, these data document the richness of a relatively unexplored component of the plant world and highlight the relevance of a whole-microbiome ecology-driven approach to botanical research and directed natural product investigations.
Keywords
plant microbiome - community composition - endophytes - epiphytes - alpha diversity - beta diversity - Actaea - Rhodiola - Ranunculaceae - CrassulaceaeSupporting Information
- Supporting Information
The number of observed features in each plant compartment, as well as a list of differentially abundant microbial taxa across host species and compartments for both bacterial and fungal datasets are available as Supporting Information.
Publication History
Received: 29 June 2024
Accepted after revision: 09 September 2024
Article published online:
24 October 2024
© 2024. Thieme. All rights reserved.
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References
- 1 Ofek-Lalzar M, Sela N, Goldman-Voronov M, Green SJ, Hadar Y, Minz D. Niche and host-associated functional signatures of the root surface microbiome. Nat Commun 2014; 5: 4950
- 2 Trivedi P, Leach JE, Tringe SG, Sa T, Singh BK. Plant-microbiome interactions: From community assembly to plant health. Nat Rev Microbiol 2020; 18: 607-621
- 3 Kabir ME, Borah A, Barman H, Sharmah B, Afzal NU, Phukan T, Kalita J, Manna P. Screening and optimization of α-glucosidase inhibitor production by potent strain of Bacillus subtilis isolated from peruyaan, fermented soy-food of Northeast India. J Food Biochem 2024; 2024: 3199103
- 4 Rana N, Rathore A, Ghabru A, Chauhan S. Endophytes: Role and applications in sustainable agriculture. Pharma Innovation 2023; 12: 139-151
- 5 Sharma G, Agarwal S, Verma K, Bhardwaj R, Mathur V. Therapeutic compounds from medicinal plant endophytes: Molecular and metabolic adaptations. J Appl Microbiol 2023; 134: lxad074
- 6 Zhao J, Zhou L, Wang J, Shan T, Lingyun Z, Liu X, Gao L. Endophytic fungi for producing bioactive compounds originally from their host plants. In: Méndez-Vilas A. editor Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology. 1st ed.. Badajoz, Spain: Formatex Research Center; 2010: 567-576
- 7 Zhang S, Zhang L, Zhu J, Chen H, Chen Z, Si T, Liu T. Genomic and metabolomic investigation of a rhizosphere isolate Streptomyces netropsis WLXQSS-4 associated with a traditional Chinese medicine. Molecules 2021; 26: 2147
- 8 Smith DR, Chapman MR. Economical evolution: Microbes reduce the synthetic cost of extracellular proteins. mBio 2010; 1: e00131-e00210
- 9 Newman DJ. Predominately uncultured microbes as sources of bioactive agents. Front Microbiol 2016; 7: 1832
- 10 Newman DJ, Cragg GM. Endophytic and epiphytic microbes as “sources” of bioactive agents. Front Chem 2015; 3: 34
- 11 Epstein SS. The phenomenon of microbial uncultivability. Curr Opin Microbiol 2013; 16: 636-642
- 12 Seo EY, Jung D, Epstein SS, Zhang W, Owen JS, Baba H, Yamamoto A, Harada M, Nakashimada Y, Kato S, Aoi Y, He S. A targeted liquid cultivation method for previously uncultured non-colony forming microbes. Front Microbiol 2023; 14: 1194466
- 13 van der Hooft JJJ, Mohimani H, Bauermeister A, Dorrestein PC, Duncan KR, Medema MH. Linking genomics and metabolomics to chart specialized metabolic diversity. Chem Soc Rev 2020; 49: 3297-3314
- 14 Staniek A, Woerdenbag HJ, Kayser O. Screening the endophytic flora of Wollemia nobilis for alternative paclitaxel sources. J Plant Interact 2010; 5: 189-195
- 15 Qiu F, McAlpine JB, Krause EC, Chen SN, Pauli GE. Pharmacognosy of black cohosh: The phytochemical and biological profile of a major botanical dietary supplement. Prog Chem Org Nat Prod 2014; 99: 1-68
- 16 Tang Y, Friesen JB, Nikolić DS, Lankin DC, McAlpine JB, Chen SN, Pauli GF. Tandem of countercurrent separation and qHNMR enables gravimetric analyses: Absolute quantitation of the Rhodiola rosea metabolome. Anal Chem 2021; 93: 11701-11709
- 17 Tang Y, Friesen JB, Lankin DC, McAlpine JB, Nikolić D, Chen SN, Pauli GF. Geraniol-derived monoterpenoid glucosides from Rhodiola rosea: resolving structures by QM-HifSA methodology. J Nat Prod 2023; 86: 256-263
- 18 Agler MT, Ruhe J, Kroll S, Morhenn C, Kim ST, Weigel D, Kemen EM. Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biol 2016; 14: e1002352
- 19 van der Heijden MG, Hartmann M. Networking in the plant microbiome. PLoS Biol 2016; 14: e1002378
- 20 Theis KR, Dheilly NM, Klassen JL, Brucker RM, Baines JF, Bosch TCG, Cryan JF, Gilbert SF, Goodnight CJ, Lloyd EA, Sapp J, Vandenkoornhuyse P, Zilber-Rosenberg I, Rosenberg E, Bordenstein SR. Getting the hologenome concept right: An Eco-evolutionary framework for hosts and their microbiomes. mSystems 2016; 1: e00028-e00116
- 21 Wink M. Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 2003; 64: 3-19
- 22 Zhang JQ, Shiyong M, Wen J, Rao GY. Phylogenetic relationships and character evolution of Rhodiola (Crassulaceae) based on nuclear ribosomal ITS and plastid trnL-F and psbA-trnH sequences. Syst Bot 2014; 39: 441-451
- 23 Dastogeer KMG, Tumpa FH, Sultana A, Akter MA, Chakraborty A. Plant microbiome–an account of the factors that shape community composition and diversity. Curr Plant Biol 2020; 23: 100161
- 24 Sauer S, Dlugosch L, Kammerer DR, Stintzing FC, Simon M. The microbiome of the medicinal plants Achillea millefolium L. and Hamamelis virginiana L. Front Microbiol 2021; 12: 696398
- 25 Belkaid Y, Naik S. Compartmentalized and systemic control of tissue immunity by commensals. Nat Immunol 2013; 14: 646-653
- 26 Cregger MA, Veach AM, Yang ZK, Crouch MJ, Vilgalys R, Tuskan GA, Schadt CW. The Populus holobiont: dissecting the effects of plant niches and genotype on the microbiome. Microbiome 2018; 6: 31
- 27 Meena KK, Kumar M, Kalyuzhnaya MG, Yandigeri MS, Singh DP, Saxena AK, Arora DK. Epiphytic pink-pigmented methylotrophic bacteria enhance germination and seedling growth of wheat (Triticum aestivum) by producing phytohormone. Antonie Van Leeuwenhoek 2012; 101: 777-786
- 28 Dourado MN, Camargo Neves AA, Santos DS, Araújo WL. Biotechnological and agronomic potential of endophytic pink-pigmented methylotrophic Methylobacterium spp. Biomed Res Int 2015; 2015: 909016
- 29 Wang Z, Zhang C, Li G, Yi X. The influence of species identity and geographic locations on gut microbiota of small rodents. Front Microbiol 2022; 13: 983660
- 30 Cervantes K, Velasco-Cruz C, Grauke LJ, Wang X, Conner P, Wells L, Bock CH, Pisani C, Randall JJ. Influence of geographical orchard location on the microbiome from the progeny of a pecan controlled cross. Plants (Basel) 2023; 12: 360
- 31 Coleman-Derr D, Desgarennes D, Fonseca-Garcia C, Gross S, Clingenpeel S, Woyke T, North G, Visel A, Partida-Martinez LP, Tringe SG. Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol 2016; 209: 798-811
- 32 Orland C, Emilson EJS, Basiliko N, Mykytczuk NCS, Gunn JM, Tanentzap AJ. Microbiome functioning depends on individual and interactive effects of the environment and community structure. ISME J 2019; 13: 1-11
- 33 Bacon CW, White JF. Functions, mechanisms and regulation of endophytic and epiphytic microbial communities of plants. Symbiosis 2016; 68: 87-98
- 34 Bernard J, Wall CB, Costantini MS, Rollins RL, Atkins ML, Cabrera FP, Cetraro ND, Feliciano CKJ, Greene AL, Kitamura PK, Olmedo-Velarde A, Sirimalwatta VNS, Sung HW, Thompson LPM, Vu HT, Wilhite CJ, Amend AS. Plant part and a steep environmental gradient predict plant microbial composition in a tropical watershed. ISME J 2021; 15: 999-1009
- 35 Wagner MR. Prioritizing host phenotype to understand microbiome heritability in plants. New Phytol 2021; 232: 502-509
- 36 Iguchi H, Yurimoto H, Sakai Y. Interactions of methylotrophs with plants and other heterotrophic bacteria. Microorganisms 2015; 3: 137-151
- 37 Naqib A, Poggi S, Wang W, Hyde M, Kunstman K, Green SJ. Making and sequencing heavily multiplexed, high-throughput 16S ribosomal RNA gene amplicon libraries using a flexible, two-stage PCR protocol. Methods Mol Biol 2018; 1783: 149-169
- 38 Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010; 7: 335-336
- 39 Kraut-Cohen J, Tripathi V, Chen Y, Gatica J, Volchinski V, Sela S, Weinberg Z, Cytryn E. Temporal and spatial assessment of microbial communities in commercial silages from bunker silos. Appl Microbiol Biotechnol 2016; 100: 6827-6835
- 40 Pryce TM, Palladino S, Kay ID, Coombs GW. Rapid identification of fungi by sequencing the ITS1 and ITS2 regions using an automated capillary electrophoresis system. Med Mycol 2003; 41: 369-381
- 41 Gat D, Reicher N, Schechter S, Alayof M, Tarn MD, Wyld BV, Zimmermann R, Rudich Y. Size-resolved community structure of bacteria and fungi transported by dust in the Middle East. Front Microbiol 2021; 12: 744117
- 42 Zhang J, Kobert K, Flouri T, Stamatakis A. PEAR: a fast and accurate Illumina paired-end read merger. Bioinformatics 2014; 30: 614-620
- 43 Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu YX, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson 2nd MS, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vázquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan Y, Wang M, Warren J, Weber KC, Williamson CHD, Willis AD, Xu ZZ, Zaneveld JR, Zhang Y, Zhu Q, Knight R, Caporaso JG. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 2019; 37: 852-857
- 44 DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 2006; 72: 5069-5072
- 45 Kõljalg U, Nilsson HR, Schigel D, Tedersoo L, Larsson KH, May TW, Taylor AFS, Jeppesen TS, Frøslev TG, Lindahl BD, Põldmaa K, Saar I, Suija A, Savchenko A, Yatsiuk I, Adojaan K, Ivanov F, Piirmann T, Pöhönen R, Zirk A, Abarenkov K. The taxon hypothesis paradigm–on the unambiguous detection and communication of Taxa. Microorganisms 2020; 8: 1910
- 46 Gonzalez A, Navas-Molina JA, Kosciolek T, McDonald D, Vázquez-Baeza Y, Ackermann G, DeReus J, Janssen S, Swafford AD, Orchanian SB, Sanders JG, Shorenstein J, Holste H, Petrus S, Robbins-Pianka A, Brislawn CJ, Wang M, Rideout JR, Bolyen E, Dillon M, Caporaso JG, Dorrestein PC, Knight R. Qiita: Rapid, web-enabled microbiome meta-analysis. Nat Methods 2018; 15: 796-798