Influence of Growth Support on the Diversity, Composition, and Functionality of Microbial Communities Associated with Tillandsia recurvata.
Epiphytic
Fence
Microbial ecology
Plant growth-promoting
Trees
Journal
Microbial ecology
ISSN: 1432-184X
Titre abrégé: Microb Ecol
Pays: United States
ID NLM: 7500663
Informations de publication
Date de publication:
16 Oct 2024
16 Oct 2024
Historique:
received:
15
07
2024
accepted:
10
10
2024
medline:
17
10
2024
pubmed:
17
10
2024
entrez:
16
10
2024
Statut:
epublish
Résumé
Tillandsia recurvata is an epiphytic plant commonly found in tropical regions and colonizes tree trunks, fences, and power wires. This plant plays an important role in interacting with trees, sharing microorganisms, and performing specific functions in the process of tree colonization. The objective of this study was to evaluate and compare the microbiomes of T. recurvata collected from two different locations (trees and fences) and two plant tissues (leaves and roots). The hypothesis of this study was that the microbiome of T. recurvata is composed of microorganisms that would provide nutritional support to compensate for the lack of nutrients in a particular growth support. The results showed significant differences in microbial diversity between trees and fences, with trees exhibiting higher richness and more complex microbial networks. Proteobacteria was the most prevalent bacterial phylum, with Actinobacteria and Sphingomonas also playing key roles in nitrogen fixation and plant growth. Fungal communities were similar across locations, with Ascomycota and Basidiomycota being predominant, but Paraconiothyrium and Nigrospora showed significant differences in abundance between trees and fences. Functional analysis indicated similar metabolic profiles across leaf and root samples, with key functions for T. recurvata including carbohydrate and amino acid metabolism, stress control, and biofertilization.
Identifiants
pubmed: 39414684
doi: 10.1007/s00248-024-02448-2
pii: 10.1007/s00248-024-02448-2
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
129Informations de copyright
© 2024. The Author(s).
Références
Bernal R, Valverde T, Hernández-Rosas L (2005) Habitat preference of the epiphyte Tillandsia recurvata (Bromeliaceae) in a semi-desert environment in Central Mexico. Can J Bot 83:1238–1247. https://doi.org/10.1139/b05-076
doi: 10.1139/b05-076
Chaves CJN, Rossatto DR (2020) Unravelling intricate interactions among atmospheric bromeliads with highly overlapping niches in seasonal systems. Plant Biol J 22:243–251. https://doi.org/10.1111/plb.13073
doi: 10.1111/plb.13073
Amarasekare P (2003) Competitive coexistence in spatially structured environments: a synthesis. Ecol Lett 6:1109–1122. https://doi.org/10.1046/j.1461-0248.2003.00530.x
doi: 10.1046/j.1461-0248.2003.00530.x
Givnish T, Millam K, Berry P, Sytsma K (2007) Phylogeny, adaptive radiation, and historical biogeography of Bromeliaceae inferred from ndhF sequence data. Aliso 23:3–26. https://doi.org/10.5642/aliso.20072301.04
doi: 10.5642/aliso.20072301.04
Benzing DH (2023) Bromeliaceae: a brief profile and some topics that warrant further inquiry. Selbyana 34:1–79
Al Ashhab A, Meshner S, Alexander-Shani R et al (2021) Temporal and spatial changes in phyllosphere microbiome of Acacia trees growing in arid environments. Front Microbiol 12:656269. https://doi.org/10.3389/fmicb.2021.656269
doi: 10.3389/fmicb.2021.656269
pubmed: 34322096
pmcid: 8312645
Zheng Y, Liu Y, Zhang J et al (2023) Dual role of endophytic entomopathogenic fungi: induce plant growth and control tomato leafminer Phthorimaea absoluta. Pest Manag Sci 79:4557–4568. https://doi.org/10.1002/ps.7657
doi: 10.1002/ps.7657
pubmed: 37431839
Maldonado JE, Gaete A, Mandakovic D et al (2022) Partners to survive: Hoffmannseggia doellii root-associated microbiome at the Atacama Desert. New Phytol 234:2126–2139. https://doi.org/10.1111/nph.18080
doi: 10.1111/nph.18080
pubmed: 35274744
Morera-Gómez Y, Alonso-Hernández CM, Armas-Camejo A, et al (2021) Pollution monitoring in two urban areas of Cuba by using Tillandsia recurvata (L.) L. and top soil samples: spatial distribution and sources. Ecol Indic 126:107667. https://doi.org/10.1016/j.ecolind.2021.107667
Joseph R, Oberle B, Thurmond J, Clore A (2020) Diverse fungal endophytes in the leaves of a widespread bromeliad, Tillandsia recurvata (L.) L
Teachey ME, Pound P, Ottesen EA, Van Stan JT (2018) Bacterial community composition of throughfall and stemflow. Front For Glob Change 1:7. https://doi.org/10.3389/ffgc.2018.00007
doi: 10.3389/ffgc.2018.00007
Pinto Júnior J, dos Santos PET, de Aguiar AV et al (2013) Melhoramento genético de espécies arbóreas na Embrapa Florestas: uma visão histórica
Benzing DH (1987) Vascular epiphytism: taxonomic participation and adaptive diversity. Annals of the Missouri Botanical Garden 183–204
Piazzetta KD, Ramsdorf WA, Maranho LT (2019) Use of airplant Tillandsia recurvata L., Bromeliaceae, as biomonitor of urban air pollution. Aerobiologia 35:125–137. https://doi.org/10.1007/s10453-018-9545-3
doi: 10.1007/s10453-018-9545-3
Cao L, Qiu Z, You J et al (2005) Isolation and characterization of endophytic Streptomycete antagonists of fusarium wilt pathogen from surface-sterilized banana roots. FEMS Microbiol Lett 247:147–152. https://doi.org/10.1016/j.femsle.2005.05.006
doi: 10.1016/j.femsle.2005.05.006
pubmed: 15935565
Caporaso JG, Lauber CL, Walters WA et al (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624. https://doi.org/10.1038/ismej.2012.8
doi: 10.1038/ismej.2012.8
pubmed: 22402401
pmcid: 3400413
White TJ, Bruns T, Lee S et al (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: a Guide to Methods and Applications 18:315–322
Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. Babraham Bioinformatics, Babraham Institute, Cambridge, United Kingdom
Edgar R (2010) Usearch. Lawrence Berkeley National Lab.(LBNL), Berkeley, CA (United States)
Didion JP, Martin M, Collins FS (2017) Atropos: specific, sensitive, and speedy trimming of sequencing reads. PeerJ 5:e3720. https://doi.org/10.7717/peerj.3720
doi: 10.7717/peerj.3720
pubmed: 28875074
pmcid: 5581536
Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:i884–i890. https://doi.org/10.1093/bioinformatics/bty560
doi: 10.1093/bioinformatics/bty560
pubmed: 30423086
pmcid: 6129281
Zhang J, Kobert K, Flouri T, Stamatakis A (2014) PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30:614–620. https://doi.org/10.1093/bioinformatics/btt593
doi: 10.1093/bioinformatics/btt593
pubmed: 24142950
Callahan BJ, McMurdie PJ, Rosen MJ et al (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581
doi: 10.1038/nmeth.3869
pubmed: 27214047
pmcid: 4927377
R Core Team (2023) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Ali A (2023) DADA2 formatted 16S rRNA gene sequences for both bacteria & archaea
Abarenkov K, Zirk A, Piirmann T, et al (2022) UNITE general FASTA release for eukaryotes
McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8:e61217
doi: 10.1371/journal.pone.0061217
pubmed: 23630581
pmcid: 3632530
Mikryukov V (2022) metagMisc: miscellaneous functions for metagenomic analysis
Andersen KS, Kirkegaard RH, Karst SM, Albertsen M (2018) ampvis2: an R package to analyse and visualise 16S rRNA amplicon data. bioRxiv
Lahti L, Shetty S (2012) microbiome R package
Oksanen J, Blanchet FG, Friendly M, et al (2019) vegan: community ecology package
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York
doi: 10.1007/978-3-319-24277-4
Revelle W (2022) psych: Procedures for psychological, psychometric, and personality research. Northwestern University, Evanston, Illinois
Csardi G, Nepusz T (2006) The igraph software package for complex network research. InterJournal Complex Systems:1695
Kleinberg JM (1999) Hubs, authorities, and communities. ACM computing surveys (CSUR) 31:5-es
Douglas GM, Maffei VJ, Zaneveld J, et al (2019) PICRUSt2: an improved and extensible approach for metagenome inference. Bioinformatics
Patz S, Gautam A, Becker M, et al (2021) PLaBAse: a comprehensive web resource for analyzing the plant growth-promoting potential of plant-associated bacteria
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550. https://doi.org/10.1186/s13059-014-0550-8
doi: 10.1186/s13059-014-0550-8
pubmed: 25516281
pmcid: 4302049
Wester S, Zotz G (2010) Growth and survival of Tillandsia flexuosa on electrical cables in Panama. J Trop Ecol 26:123–126. https://doi.org/10.1017/S0266467409990459
doi: 10.1017/S0266467409990459
Aguilar-Cruz Y, Milke F, Leinberger J et al (2022) Diversity and putative metabolic function of prokaryotic communities in tank bromeliads along an elevation gradient in tropical Mexico. Front Microbiol 13:945488. https://doi.org/10.3389/fmicb.2022.945488
doi: 10.3389/fmicb.2022.945488
pubmed: 36312956
pmcid: 9608151
Brandt FB, Martinson GO, Conrad R (2017) Bromeliad tanks are unique habitats for microbial communities involved in methane turnover. Plant Soil 410:167–179. https://doi.org/10.1007/s11104-016-2988-9
doi: 10.1007/s11104-016-2988-9
Barka EA, Vatsa P, Sanchez L et al (2016) Taxonomy, physiology, and natural products of Actinobacteria. Microbiol Mol Biol Rev 80:1–43. https://doi.org/10.1128/MMBR.00019-15
doi: 10.1128/MMBR.00019-15
pubmed: 26609051
Kielak AM, Barreto CC, Kowalchuk GA, et al (2016) The ecology of Acidobacteria: moving beyond genes and genomes. Front Microbiol 7:. https://doi.org/10.3389/fmicb.2016.00744
Mazoyon C, Hirel B, Pecourt A, et al (2023) Sphingomonas sediminicola is an endosymbiotic bacterium able to induce the formation of root nodules in pea (Pisum sativum L.) and to enhance plant biomass production. Microorganisms 11:199. https://doi.org/10.3390/microorganisms11010199
Brighigna L, Montaini P, Favilli F, Trejo AC (1992) Role of the nitrogen-fixing bacterial microflora in the epiphytism of Tillandsia (Bromeliaceae). Am J Bot 79:723–727
Pankratov TA, Grouzdev DS, Patutina EO et al (2020) Lichenibacterium ramalinae gen. nov, sp. nov., Lichenibacterium minor sp. nov., the first endophytic, beta-carotene producing bacterial representatives from lichen thalli and the proposal of the new family Lichenibacteriaceae within the order Rhizobiales. Antonie Van Leeuwenhoek 113:477–489. https://doi.org/10.1007/s10482-019-01357-6
doi: 10.1007/s10482-019-01357-6
pubmed: 31741189
Hagee D, Abu Hardan A, Botero J, Arnone JT (2020) Genomic clustering within functionally related gene families in Ascomycota fungi. Comput Struct Biotechnol J 18:3267–3277. https://doi.org/10.1016/j.csbj.2020.10.020
doi: 10.1016/j.csbj.2020.10.020
pubmed: 33209211
pmcid: 7653285
Mattila H, Österman-Udd J, Mali T, Lundell T (2022) Basidiomycota fungi and ROS: genomic perspective on key enzymes involved in generation and mitigation of reactive oxygen species. Front Fungal Biol 3:837605. https://doi.org/10.3389/ffunb.2022.837605
doi: 10.3389/ffunb.2022.837605
pubmed: 37746164
pmcid: 10512322
Martins Alves N, Araújo Guimarães R, Silva Costa Guimarães S et al (2021) A Trojan horse approach for white mold biocontrol: Paraconiothyrium endophytes promotes grass growth and inhibits Sclerotiniasclerotiorum. Biol Control 160:104685. https://doi.org/10.1016/j.biocontrol.2021.104685
doi: 10.1016/j.biocontrol.2021.104685
Safwan S, Hsiao G, Lee T-H, Lee C-K (2021) Bioactive compounds from an endophytic fungi Nigrospora aurantiaca. Bot Stud 62:18. https://doi.org/10.1186/s40529-021-00324-7
doi: 10.1186/s40529-021-00324-7
pubmed: 34698886
pmcid: 8548483
López-Moral A, Lovera M, Antón-Domínguez BI et al (2023) Effects of cultivar susceptibility, fruit maturity, and natural wounds on the infection of English walnut (Juglans regia L.) fruits by Botryosphaeriaceae and Diaporthe fungi. J Plant Pathol 105:1391–1401. https://doi.org/10.1007/s42161-023-01492-0
doi: 10.1007/s42161-023-01492-0
Félix CR, Da Silva Nascimento BE, Valente P, Landell MF (2022) Different plant compartments, different yeasts: the example of the bromeliad phyllosphere. Yeast 39:363–400. https://doi.org/10.1002/yea.3804
doi: 10.1002/yea.3804
pubmed: 35715939
de Souza R, Ambrosini A, Passaglia LMP (2015) Plant growth-promoting bacteria as inoculants in agricultural soils. Genet Mol Biol 38:401–419. https://doi.org/10.1590/S1415-475738420150053
doi: 10.1590/S1415-475738420150053
pubmed: 26537605
pmcid: 4763327
Gao M, Tang F, Wang K et al (2022) Heterogeneity of humic/fulvic acids derived from composts explains the differences in accelerating soil Cd-hyperaccumulation by Sedum alfredii. J Environ Manage 301:113837. https://doi.org/10.1016/j.jenvman.2021.113837
doi: 10.1016/j.jenvman.2021.113837
pubmed: 34592668