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Microbial Diversity in Cultivated and Feral Vanilla Vanilla planifolia Orchids Affected by Stem and Rot Disease

Abstract

The worldwide production of vanilla, a native orchid from Mexico, is greatly affected by stem and root rot disease (SRD), typically associated with Fusarium oxysporum fungi. We hypothesized that the presence of Fusarium species in vanilla is not sufficient for the plant to express symptoms of the disease. We described the taxonomic composition of endophytic microbiomes in symptomatic and asymptomatic vanilla plants using 16S and ITS rDNA metabarcoding, and ITS Sanger sequences generated from fungal isolates. We compared the bacterial and fungal diversity in vanilla plants from a long-term plantation, and from feral plants found near abandoned plantations that did not present SRD symptoms. No significant differences were found in the species richness of the bacterial and fungal microbiome among feral, or asymptomatic and symptomatic cultivated vanilla. However, significant differences were detected in both fungal and bacterial diversity from different organs in the same plant, with roots being more diverse than stems. We found that Proteobacteria and Actinobacteria, as well as the fungal families Nectriaceae and Xylariaceae, constitute the core of the vanilla microbiome that inhabits the root and stem of both cultivated and feral plants. Our work provides information on the microbial diversity associated to root and stem rot in vanilla and lays the groundwork for a better understanding of the role of the microbiome in vanilla fungal diseases.

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Data Availability

The nucleotide sequence data reported are available in the DDBJ/EMBL/GenBank databases under the accession number(s) as follows:

Isolate ID Taxonomical classification GB accession
VPI_S15 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Xylariomycetidae; Xylariales; Xylariaceae; Daldinia MZ270645
VPI_A20 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Xylariomycetidae; Xylariales; Xylariaceae; Daldinia MZ270646
VPI_S31 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Xylariomycetidae; Xylariales; Xylariaceae; Daldinia MZ270647
VPI_S63 Fungi; Dikarya; Basidiomycota; Agaricomycotina; Agaricomycetes; Agaricomycetes sbc Incertae sedis; Polyporales; Irpicaceae; Ceriporia MZ270648
VPI_S16 Fungi; Dikarya; Basidiomycota; Agaricomycotina; Agaricomycetes; Agaricomycetes sbc Incertae sedis; Polyporales; Irpicaceae MZ270649
VPI_S35 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Hypocreomycetidae; Hypocreales; Bionectriaceae; Clonostachys MZ270650
VPI_S51 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Hypocreomycetidae; Hypocreales; Bionectriaceae; Clonostachys MZ270651
VPI_S1 Fungi; Dikarya; Ascomycota; Pezizomycotina; Eurotiomycetes; Eurotiomycetidae; Eurotiales; Aspergillaceae; Penicillium MZ270652
VPI_A12 Fungi; Dikarya; Ascomycota MZ270653
VPI_S18b Fungi; Dikarya; Ascomycota MZ270654
VPI_A29 Fungi; Dikarya; Ascomycota MZ270655
VPI_S65 Fungi; Dikarya; Ascomycota MZ270656
VPI_S13 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Xylariomycetidae; Xylariales MZ270657
VPI_S19 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Xylariomycetidae; Xylariales MZ270658
VPI_S21 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Xylariomycetidae; Xylariales MZ270659
VPI_S28 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Xylariomycetidae; Xylariales MZ270660
VPI_S41 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Xylariomycetidae; Xylariales MZ270661
VPI_S42 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Xylariomycetidae; Xylariales MZ270662
VPI_S46 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Xylariomycetidae; Xylariales MZ270663
VPI_A47 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Xylariomycetidae; Xylariales MZ270664
VPI_S52 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Xylariomycetidae; Xylariales MZ270665
VPI_S5 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Xylariomycetidae; Xylariales MZ270666
VPI_S24 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Xylariomycetidae; Xylariales; Xylariaceae; Xylaria MZ270667
VPI_S30 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Xylariomycetidae; Xylariales; Xylariaceae; Xylaria MZ270668
VPI_S32 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Xylariomycetidae; Xylariales; Xylariaceae; Xylaria MZ270669
VPI_S54 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Xylariomycetidae; Xylariales; Xylariaceae; Xylaria MZ270670
VPI_A11 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Xylariomycetidae; Xylariales; Xylariaceae; Hypoxylon MZ270671
VPI_S14 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Xylariomycetidae; Xylariales; Xylariaceae; Hypoxylon MZ270672
VPI_S17b Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Hypocreomycetidae; Hypocreales; Nectriaceae; Fusarium MZ270673
VPI_A22 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Hypocreomycetidae; Hypocreales; Nectriaceae; Fusarium MZ270674
VPI_S45 Fungi; Dikarya; Ascomycota MZ270675
VPI_A39 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Sordariomycetes sbc Incertae sedis; Trichosphaeriales; Trichosphaeriaceae; Nigrospora MZ270676
VPI_A3 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Sordariomycetes sbc Incertae sedis; Trichosphaeriales; Trichosphaeriaceae; Nigrospora MZ270677
VPI_S10 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Hypocreomycetidae; Hypocreales; Stachybotryaceae; Myxospora MZ270678
VPI_S17 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Hypocreomycetidae; Hypocreales; Stachybotryaceae; Myxospora MZ270679
VPI_S38 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Hypocreomycetidae; Hypocreales; Stachybotryaceae; Myxospora MZ270680
VPI_S66 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Hypocreomycetidae; Hypocreales; Stachybotryaceae; Myxospora MZ270681
VPI_A25 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Hypocreomycetidae; Hypocreales; Stachybotryaceae; Myxospora MZ270682
VPI_S64 Fungi; Dikarya; Ascomycota; Pezizomycotina; Dothideomycetes; Pleosporomycetidae MZ270683
VPI_S70 Fungi; Dikarya; Ascomycota MZ270684
VPI_S72 Fungi; Dikarya; Ascomycota MZ270685
VPI_A73 Fungi; Dikarya; Ascomycota MZ270686
VPI_S8 Fungi; Dikarya; Ascomycota MZ270687
VPI_A1a Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Hypocreomycetidae; Hypocreales; Nectriaceae; Gibberella MZ270702
VPI_S1b Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Hypocreomycetidae; Hypocreales; Nectriaceae; Gibberella MZ270688
VPI_A23 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Hypocreomycetidae; Hypocreales; Nectriaceae; Gibberella MZ270689
VPI_A27 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Hypocreomycetidae; Hypocreales; Nectriaceae; Gibberella MZ270690
VPI_S2a Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Hypocreomycetidae; Hypocreales; Nectriaceae; Gibberella MZ270691
VPI_S62 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Hypocreomycetidae; Hypocreales MZ270692
VPI_S7 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Hypocreomycetidae; Hypocreales MZ270693
VPI_A9 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Hypocreomycetidae; Hypocreales MZ270694
VPI_S26 Fungi; Dikarya; Ascomycota; Pezizomycotina; Sordariomycetes; Hypocreomycetidae MZ270695
VPI_S33 Fungi; Dikarya; Ascomycota; Pezizomycotina MZ270696
VPI_A34 Fungi; Dikarya; Ascomycota; Pezizomycotina; Dothideomycetes; Pleosporomycetidae; Pleosporales; Biatriosporaceae; Biatriospora MZ270697
VPI_S36 Fungi; Dikarya; Ascomycota; Pezizomycotina; Dothideomycetes; Pleosporomycetidae; Pleosporales; Biatriosporaceae; Biatriospora MZ270698
VPI_S53 Fungi; Dikarya; Ascomycota; Pezizomycotina; Dothideomycetes; Pleosporomycetidae; Pleosporales; Biatriosporaceae; Biatriospora MZ270699
VPI_A55 Fungi; Dikarya; Ascomycota; Pezizomycotina; Dothideomycetes; Pleosporomycetidae; Pleosporales; Biatriosporaceae; Biatriospora MZ270700
VPI_A59 Fungi; Dikarya; Ascomycota; Pezizomycotina; Dothideomycetes; Pleosporomycetidae; Pleosporales; Pleosporales fam Incertae sedis; Nigrograna MZ270701
Sample name SPUID Organism Tax ID BioProject GB accession
V1 V1 Plant metagenome 1297885 PRJNA756110 SAMN20855179
V2 V2 Plant metagenome 1297885 PRJNA756110 SAMN20855180
V3 V3 Plant metagenome 1297885 PRJNA756110 SAMN20855181
V4 V4 Plant metagenome 1297885 PRJNA756110 SAMN20855182
V5 V5 Plant metagenome 1297885 PRJNA756110 SAMN20855183
V6 V6 Plant metagenome 1297885 PRJNA756110 SAMN20855184
V7 V7 Plant metagenome 1297885 PRJNA756110 SAMN20855185
V8 V8 Plant metagenome 1297885 PRJNA756110 SAMN20855186
V9 V9 Plant metagenome 1297885 PRJNA756110 SAMN20855187
V10 V10 Plant metagenome 1297885 PRJNA756110 SAMN20855188
V11 V11 Plant metagenome 1297885 PRJNA756110 SAMN20855189
V12 V12 Plant metagenome 1297885 PRJNA756110 SAMN20855190
V13 V13 Plant metagenome 1297885 PRJNA756110 SAMN20855191
V14 V14 Plant metagenome 1297885 PRJNA756110 SAMN20855192
V15 V15 Plant metagenome 1297885 PRJNA756110 SAMN20855193
V16 V16 Plant metagenome 1297885 PRJNA756110 SAMN20855194

Code Availability

In-house scripts are available upon request.

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Acknowledgements

We are deeply grateful to Mr. Raul Degetau and Mr. Adrian Schravesade, owners of Veinte Soles® and ONZA® vanilla plantations for assisting with this project. Funding for this project was provided to ACJ by a UCMEXUS grant and FBG by Conacyt, Mexico (grant No. 285746) and the Royal Society of the United Kingdom, Newton Advanced Fellowship (NAF\R2\180631).

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ICV and AHMS completed the field work, extracted DNA, generated the microbiological live collection, and analyzed the data. CT analyzed the data and contributed significantly to the revision of the manuscript, as well as conceptually to the methods. JHH and RD assisted in the field and are the owners of live vanilla collections or feral plants where all the samples were obtained for this study. FBG assisted in the field and contributed to the microbiological live collection, as well as provided partial funding. ACJ conceived the study, provided funding, led sample collections in the field and wrote part of the manuscript.

Corresponding author

Correspondence to Angélica Cibrián-Jaramillo.

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No conflict of interest or competing interests.

Supplementary Information

Below is the link to the electronic supplementary material.

248_2021_1876_MOESM1_ESM.pdf

Supplementary file1 Fig. S1 Phylogenetic tree of Fusarium genus ITS sequences. Alignments were performed in Muscle [22], verified with Gblocks [23] and tree generated by maximum likelihood trees in MegaX [24] using the Tamura-Nei substitution model (selected based on the lowest AIC scores) and 1000 bootstrap replicates (PDF 796 kb)

248_2021_1876_MOESM2_ESM.pdf

Supplementary file2 Fig. S2 Phylogenetic tree of Xylariaceae family ITS sequences. Alignments were performed in Muscle (Edgar, 2004), verified with Gblocks [23] and tree generated by maximum likelihood trees in MegaX [24] using the Tamura-Nei substitution model (selected based on the lowest AIC scores) and 1000 bootstrap replicates (PDF 615 kb)

248_2021_1876_MOESM3_ESM.pdf

Supplementary file3 Fig. S3 Differential heat tree matrices illustrate change in (A) bacterial) and (B) fungal relative abundances between conditions at the family level, for taxa with relative abundance > 0.01% of total read count per sample. The size of nodes in the gray cladograms depicts the number of taxa identified at each taxonomic level. The smaller cladograms represent pairwise comparisons between conditions: an orange node indicates higher abundance in the condition stated horizontally, while a blue-green node indicates a higher abundance in the condition stated vertically. Significant differences according to Wilcoxon Rank Sum tests with FDR correction for multiple comparisons are illustrated in Figure 3 (PDF 4.29 mb)

Supplementary file4 Table S1 Endophytic fungi isolated from Vanilla planifolia (CSV 57 kb)

Supplementary file5 (XLSX 38131 kb)

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Carbajal-Valenzuela, I.A., Muñoz-Sanchez, A.H., Hernández-Hernández, J. et al. Microbial Diversity in Cultivated and Feral Vanilla Vanilla planifolia Orchids Affected by Stem and Rot Disease. Microb Ecol (2021). https://doi.org/10.1007/s00248-021-01876-8

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Keywords

  • Fusarium
  • Metabarcoding
  • Microbiome
  • Pathogen resistance
  • Vanilla planifolia