A First Draft of the Core Fungal Microbiome of Schedonorus arundinaceus with and without Its Fungal Mutualist Epichloë coenophiala
Abstract
:1. Introduction
- What species are present?
- What species were present in all or most plants over time (which we refer to as the draft “core microbiome”)?
- Were these fungal communities influenced by the presence of the E. coenophiala endophyte?
- Were these fungal communities different between plants infected with different strains of the Epichloë endophyte?
- Were these fungal communities correlated with surrogates of plant fitness?
2. Methods
2.1. Field Samples
2.2. DNA Extraction and Sequencing
2.3. Epichloë Concentration
2.4. Bioinformatics
2.5. Statistical Analyses
3. Results
3.1. Taxonomic Variability across Epichloë Treatments and Years
3.2. ASV Co-Occurrences
3.3. Fungal Community Structure
3.4. Draft Core Microbiome
3.5. Guilds
3.6. Differential Reads
3.7. Epichloë coenophiala Concentrations and Plant Fitness
3.8. Relationship between Core ASVs, Plant Fitness, and Epichloë Concentrations
4. Discussion
4.1. Taxonomy
4.2. Effect of Epichloë and Comparisons with Previous Research
4.3. Variation over Time
4.4. Plant Fitness
4.5. Limitations
4.6. Conclusions and Future Directions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Phylum (P), Class (C), Order(O) | Family | Genus | Species | ASVs Raw | ASVs Rarefied | Reads Raw | Reads Rarefied |
---|---|---|---|---|---|---|---|
P: Ascomycota | 0.680 | 0.670 | 0.896 | 0.895 | |||
C: Dothideomycetes | 0.418 | 0.411 | 0.662 | 0.649 | |||
O: Capnodiales | 0.037 | 0.039 | 0.047 | 0.041 | |||
Cladosporiaceae | Cladosporium | cladosporioides | 0.017 | 0.018 | |||
Neodevriesiaceae | Neodevriesia | poagena | 0.004 | 0.005 | |||
Teratosphaeriaceae | 0.011 | ||||||
O: Pleosporales | 0.352 | 0.343 | 0.633 | 0.618 | |||
Cucurbitariaceae | 0.059 | 0.062 | |||||
Cucurbitariaceae | Pyrenochaetopsis | 0.059 | 0.062 | ||||
Pyrenochaetopsis | leptospora | 0.036 | 0.038 | ||||
Coniothyriaceae | Coniothyrium | crepinianum | 0.003 | ||||
Didymellaceae | 0.017 | 0.020 | 0.060 | 0.074 | |||
Neoascochyta | 0.049 | 0.062 | |||||
Neoascochyta | tardicrescens | 0.049 | 0.060 | ||||
Didymosphaeriaceae | 0.012 | 0.062 | 0.061 | ||||
Paraphaeosphaeria | 0.062 | 0.061 | |||||
Paraphaeosphaeria | rosae | 0.014 | 0.012 | ||||
Lentitheciaceae | 0.021 | 0.020 | 0.030 | 0.034 | |||
Keissleriella | 0.009 | 0.010 | |||||
Keissleriella | quadriseptata | 0.004 | |||||
Phaeosphaeriaceae | 0.204 | 0.188 | 0.307 | 0.275 | |||
Neosetophoma | samararum | 0.004 | |||||
Parastagonospora | 0.0253 | 0.244 | 0.0396 | 0.0299 | |||
Phaeosphaeria | 0.017 | 0.019 | |||||
Piniphoma | wesendahlina | 0.019 | 0.020 | ||||
Septoriella | 0.044 | 0.032 | 0.091 | 0.085 | |||
Septoriella | phragmitis | 0.042 | 0.031 | 0.092 | 0.087 | ||
Pleosporaceae | 0.015 | 0.017 | 0.028 | 0.028 | |||
Alternaria | 0.009 | 0.011 | 0.028 | 0.028 | |||
Alternaria | infectoria | 0.005 | 0.006 | ||||
C: Eurotiomycetes | 0.028 | 0.029 | 0.023 | 0.023 | |||
O: Chaetothyriales | 0.027 | 0.028 | 0.023 | 0.023 | |||
C: Lecanoromycetes | 0.016 | 0.018 | 0.064 | 0.063 | |||
O: Ostropales | 0.013 | 0.063 | 0.063 | ||||
Gomphillaceae | 0.043 | 0.042 | |||||
Corticifraga | 0.043 | 0.041 | |||||
Corticifraga | peltigerae | 0.004 | 0.043 | 0.041 | |||
Stictidaceae | Neofitzroyomyces | 0.020 | 0.021 | ||||
Neofitzroyomyces | nerii | 0.005 | 0.006 | 0.020 | 0.021 | ||
C: Leotiomycetes | 0.057 | 0.064 | 0.093 | 0.108 | |||
O: Helotiales | 0.053 | 0.061 | 0.093 | 0.108 | |||
Helotiaceae | 0.053 | 0.061 | 0.093 | 0.108 | |||
Articulospora | 0.012 | 0.014 | 0.020 | ||||
Articulospora | proliferata | 0.012 | 0.014 | 0.020 | 0.020 | ||
Hyaloscyphaceae | 0.012 | 0.015 | |||||
C: Saccharomycetes | 0.012 | ||||||
O: Saccharomycetales | 0.012 | ||||||
Metschnikowiaceae | Metschnikowia | 0.011 | |||||
C: Sordariomycetes | 0.072 | 0.075 | 0.046 | 0.042 | |||
O: Glomerellales | 0.020 | 0.017 | |||||
O: Hypocreales | 0.029 | 0.030 | 0.014 | 0.016 | |||
O: Xylariales | 0.007 | ||||||
P: Basidiomycota | 0.254 | 0.272 | 0.100 | 0.100 | |||
C: Agaricomycetes | 0.112 | 0.119 | 0.059 | 0.055 | |||
O: Agaricales | 0.036 | 0.038 | |||||
Psathyrellaceae | 0.011 | 0.012 | |||||
O: Cantharellales | 0.012 | 0.005 | |||||
O: Corticiales | 0.032 | 0.039 | 0.047 | 0.041 | |||
Corticiaceae | 0.032 | 0.038 | 0.047 | 0.041 | |||
Laetisaria | 0.011 | ||||||
Laetisaria | lichenicola | 0.009 | 0.011 | ||||
Limonomyces | 0.014 | 0.017 | 0.032 | 0.032 | |||
C: Cystobasidiomycetes | 0.022 | 0.023 | 0.003 | 0.003 | |||
C: Microbotryomycetes | 0.012 | 0.013 | 0.002 | 0.002 | |||
C: Tremellomycetes | 0.065 | 0.077 | 0.034 | 0.038 | |||
O: Tremellales | 0.049 | 0.056 | 0.028 | 0.032 | |||
Bulleribasidiaceae | 0.030 | 0.034 | 0.025 | 0.029 | |||
Dioszegia | 0.010 | 0.012 | |||||
Vishniacozyma | 0.014 | 0.016 | 0.022 | ||||
Vishniacozyma | dimennae | 0.004 | 0.004 | ||||
Vishniacozyma | tephrensis | 0.010 | 0.012 | ||||
Vishniacozyma | victoriae | 0.004 | 0.004 | ||||
P: Chytridiomycota | 0.013 | 0.014 | 0.003 | 0.003 | |||
C: Spizellomycetes | 0.013 | 0.003 | 0.003 | ||||
O: Spizellomycetales | 0.013 | ||||||
P: Mortierellomycota | 0.002 | 0.001 | 0.000 | 0.000 | |||
P: Mucoromycota | 0.000 | 0.000 | 0.000 | 0.000 | |||
P: Olpidiomycota | 0.000 | 0.000 | 0.000 | ||||
P: Rozellomycota | 0.000 | 0.000 | 0.000 |
Epichloë Treatment | 2017 Only | 2018 Only | Both Years | Subtotal |
---|---|---|---|---|
E+ only | 264 | 315 | 33 | 612 |
E− only | 272 | 264 | 45 | 581 |
AR542 only | 232 | 191 | 24 | 447 |
E+, E− only | 42 | 15 | 15 | 72 |
E+, AR542 only | 27 | 20 | 6 | 53 |
E−, AR542 only | 32 | 11 | 9 | 52 |
E+, E−, AR542 | 30 | 16 | 302 | 348 |
Subtotal | 899 | 832 | 434 | 2165 |
A. 2017 | |||||||
---|---|---|---|---|---|---|---|
Source | df | SS | MS | F | P | s | |
Epichloë | 2 | 0.34 | 0.17 | 1.04 | 0.04 | 0.3873 | 1.37 |
Row | 16 | 3.15 | 0.20 | 1.20 | 0.41 | 0.0144 | 6.12 |
Column | 2 | 0.45 | 0.236 | 1.37 | 0.06 | 0.0349 | 4.84 |
Residuals | 23 | 3.78 | 0.16 | 0.49 | |||
Total | 43 | 7.72 | 1.00 | ||||
B. 2018 | |||||||
Source | df | SS | MS | F | P | s | |
Epichloë | 2 | 0.39 | 0.19 | 1.42 | 0.05 | 0.0453 | 4.46 |
Row | 16 | 3.03 | 0.19 | 1.39 | 0.42 | 0.0007 | 10.48 |
Column | 2 | 0.48 | 0.24 | 1.76 | 0.07 | 0.0061 | 7.35 |
Residuals | 23 | 3.26 | 0.14 | 0.46 | |||
Total | 43 | 7.16 | 1.00 |
2017 Plants | 2018 Plants | Proportion | Epichloë | Year | Intx | Consistent Correlations | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Taxonomic Identity | ASV | AR542 | E+ | E− | AR542 | E+ | E− | Reads | p-Value | p-Value | p-Value | Tiller # | Seed # | [Epichloë] | Guild | |
plants | family: Phaeosphaeriaceae | ASV1 | 13 | 15 | 16 | 13 | 16 | 16 | 0.095 | 3.04 × 10 | 1.11 × 10 | 9.64 × 10 | ||||
family: Phaeosphaeriaceae | ASV2 | 13 | 15 | 16 | 13 | 16 | 16 | 0.082 | 4.55 × 10 | 9.80 × 10 | 7.37 × 10 | |||||
family: Didymosphaeriaceae | ASV3 | 13 | 15 | 16 | 13 | 16 | 16 | 0.057 | 8.27 × 10 | 1.06 × 10 | 3.89 × 10 | |||||
order: Pleosporales | ASV4 | 13 | 15 | 16 | 13 | 16 | 16 | 0.057 | 5.31 × 10 | 2.39 × 10 | 2.33 × 10 | |||||
Neoascochyta tardicrescens | ASV5 | 13 | 15 | 16 | 13 | 16 | 16 | 0.049 | 6.80 × 10 | 1.94 × 10 | 9.22 × 10 | |||||
Corticifraga peltigerae | ASV6 | 13 | 15 | 16 | 13 | 16 | 16 | 0.039 | 2.07 × 10 | 9.99 × 10 | 5.81 × 10 | |||||
Pyrenochaetopsis leptospora | ASV7 | 13 | 15 | 16 | 13 | 16 | 16 | 0.036 | 7.71 × 10 | 4.86 × 10 | 7.61 × 10 | |||||
family: Lentitheciaceae | ASV9 | 13 | 15 | 16 | 13 | 16 | 16 | 0.027 | 5.00 × 10 | 7.65 × 10 | 6.05 × 10 | |||||
Volucrispora graminea | ASV10 | 13 | 15 | 16 | 13 | 16 | 16 | 0.026 | 7.01 × 10 | 4.09 × 10 | 9.54 × 10 | |||||
genus: Pyrenochaetopsis | ASV11 | 13 | 15 | 16 | 13 | 16 | 16 | 0.024 | 8.45 × 10 | 2.51 × 10 | 8.04 × 10 | |||||
Cladosporium cladosporioides | ASV15 | 13 | 15 | 16 | 13 | 16 | 16 | 0.018 | 6.21 × 10 | 7.86 × 10 | 5.40 × 10 | E,PP,WS | ||||
order: Chaetothyriales | ASV19 | 13 | 15 | 16 | 13 | 16 | 16 | 0.014 | 4.20 × 10 | 5.92 × 10 | 6.93 × 10 | |||||
Epicoccum nigrum | ASV32 | 13 | 15 | 16 | 13 | 16 | 16 | 0.006 | 4.58 × 10 | 4.15 × 10 | 7.52 × 10 | E,PP | ||||
plant | genus: Colletotrichum | ASV12 | 13 | 14 | 16 | 13 | 16 | 16 | 0.015 | 8.58 × 10 | 6.27 × 10 | 6.65 × 10 | E,PP | |||
genus: Parastagonospora | ASV18 | 13 | 15 | 15 | 13 | 15 | 16 | 0.012 | 5.54 × 10 | 5.56 × 10 | 3.88 × 10 | |||||
Alternaria rosae | ASV21 | 13 | 15 | 15 | 13 | 16 | 16 | 0.011 | 4.85 × 10 | 2.25 × 10 | 6.46 × 10 | AP,E,PP,WS | ||||
Alternaria alternata | ASV27 | 13 | 15 | 15 | 13 | 16 | 16 | 0.008 | 4.00 × 10 | 4.64 × 10 | 8.69 × 10 | AP,E,PP,WS | ||||
Vishniacozyma tephrensis | ASV29 | 13 | 15 | 16 | 12 | 16 | 16 | 0.008 | 7.33 × 10 | 2.00 × 10 | 7.25 × 10 | |||||
genus: Parastagonospora | ASV28 | 13 | 14 | 15 | 13 | 16 | 16 | 0.007 | 6.26 × 10 | 1.18 × 10 | 4.15 × 10 | |||||
Vishniacozyma tephrensis | ASV61 | 13 | 15 | 16 | 12 | 16 | 15 | 0.003 | ||||||||
family: Tubeufiaceae | ASV76 | 13 | 15 | 15 | 13 | 16 | 15 | 0.002 | 8.09 × 10 | 2.61 × 10 | 6.42 × 10 | |||||
plants | Vishniacozyma victoriae | ASV50 | 13 | 15 | 16 | 11 | 16 | 15 | 0.004 | 3.37 × 10 | 8.44 × 10 | 3.29 × 10 | ||||
Phialophora livistonae | ASV62 | 11 | 15 | 15 | 12 | 16 | 15 | 0.003 | 3.88 × 10 | 4.85 × 10 | 2.92 × 10 | |||||
Devriesia pseudoamericana | ASV67 | 12 | 15 | 14 | 11 | 16 | 15 | 0.002 | ||||||||
order: Pleosporales | ASV68 | 11 | 13 | 15 | 12 | 15 | 14 | 0.002 | 2.93 × 10 | 4.81 × 10 | 9.01 × 10 | |||||
Epicoccum nigrum | ASV95 | 11 | 14 | 16 | 12 | 14 | 15 | 0.001 | 9.93 × 10 | 1.95 × 10 | 3.61 × 10 | E,PP | ||||
plants | family: Phaeosphaeriaceae | ASV17 | 13 | 14 | 15 | 11 | 13 | 13 | 0.011 | 2.90 × 10 | 3.51 × 10 | 9.22 × 10 | ||||
Articulospora proliferata | ASV23 | 12 | 15 | 15 | 13 | 13 | 14 | 0.010 | 1.78 × 10 | 1.61 × 10 | 4.30 × 10 | |||||
Alternaria infectoria | ASV47 | 10 | 15 | 13 | 12 | 13 | 15 | 0.004 | AP,E,PP,WS | |||||||
genus: Cyphellophora | ASV53 | 10 | 15 | 15 | 10 | 13 | 15 | 0.003 | AP | |||||||
Paraophiobolus plantaginis | ASV144 | 10 | 12 | 13 | 10 | 15 | 14 | 0.001 | ||||||||
plants | Piniphoma wesendahlina | ASV13 | 10 | 11 | 12 | 12 | 12 | 13 | 0.020 | |||||||
genus: Cryptocoryneum | ASV48 | 9 | 11 | 13 | 12 | 12 | 15 | 0.004 | ||||||||
Alternaria infectoria | ASV60 | 11 | 13 | 12 | 12 | 16 | 16 | 0.003 | pp | |||||||
Vishniacozyma dimennae | ASV84 | 13 | 15 | 16 | 9 | 13 | 14 | 0.002 | 3.47 × 10 | 1.03 × 10 | 2.61 × 10 | |||||
genus: Acremonium | ASV93 | 12 | 13 | 13 | 13 | 12 | 14 | 0.001 | ||||||||
plants | Neofitzroyomyces nerii | ASV30 | 10 | 10 | 13 | 9 | 12 | 13 | 0.008 | |||||||
Fusarium langsethiae | ASV56 | 9 | 14 | 11 | 10 | 15 | 16 | 0.004 | AP,E,PP,WS | |||||||
genus: Parastagonospora | ASV55 | 13 | 12 | 11 | 12 | 14 | 13 | 0.003 | gpp | |||||||
family: Lentitheciaceae | ASV78 | 12 | 14 | 15 | 10 | 11 | 11 | 0.003 | ||||||||
Articulospora proliferata | ASV72 | 9 | 15 | 12 | 9 | 11 | 14 | 0.002 | ||||||||
Paraphaeosphaeria michotii | ASV90 | 8 | 14 | 11 | 13 | 16 | 15 | 0.002 | pp | |||||||
Chrysozyma griseoflava | ASV110 | 11 | 13 | 15 | 11 | 13 | 11 | 0.001 | ||||||||
sum: | 0.691 |
Different across Epichloë Treatment | Different across Years | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
ASV | Taxonomy | E− | E+ | AR542 | 2017 | 2018 | |||||
Reads | Plants | Reads | Plants | Reads | Plants | Reads | Plants | Reads | Plants | ||
ASV1 | Family: Phaeosphaeriaceae | 19,623 | 44 | 82,628 | 45 | ||||||
ASV2 | Septoriella phragmitis | 30,098 | 44 | 57,643 | 45 | ||||||
ASV12 | Genus: Colletotrichum | 1589 | 43 | 14,207 | 45 | ||||||
ASV15 | Cladosporium cladosporioides | 5562 | 44 | 13,512 | 45 | ||||||
ASV17 | Family: Phaeosphaeriaceae | 9803 | 43 | 2097 | 39 | ||||||
ASV21 | Alternaria rosae | 2777 | 43 | 9361 | 45 | ||||||
ASV29 | Vishniacozyma tephrensis | 6888 | 44 | 1502 | 44 | ||||||
ASV41 | Order: Pleosporales | 304 | 17 | 3072 | 36 | ||||||
ASV46 | Genus: Dioszegia | 3839 | 44 | 177 | 31 | ||||||
ASV50 | Vishniacozyma victoriae | 3179 | 44 | 1290 | 42 | ||||||
ASV60 | Alternaria infectoria | 1096 | 36 | 2431 | 44 | ||||||
ASV61 | Vishniacozyma tephrensis | 2667 | 44 | 1075 | 43 | ||||||
ASV70 | Colletotrichum eleusines | 152 | 15 | 942 | 30 | ||||||
ASV78 | Family: Lentitheciaceae | 2263 | 41 | 432 | 34 | ||||||
ASV84 | Vishniacozyma dimennae | 1591 | 44 | 402 | 37 | ||||||
ASV88 | Order: Pleosporales | 1157 | 42 | 348 | 32 | ||||||
ASV90 | Paraphaeosphaeria michotii | 581 | 34 | 1047 | 44 | ||||||
ASV98 | Ramularia collo-cygni | 392 | 30 | 805 | 43 | ||||||
ASV108 | Alfaria ossiformis | 223 | 17 | 988 | 34 | ||||||
ASV114 | Cystofilobasidium macerans | 1340 | 42 | 9 | 6 | ||||||
ASV125 | Coniothyrium crepinianum | 31 | 3 | 834 | 18 | ||||||
ASV137 | Dioszegia rishiriensis | 930 | 40 | 74 | 19 | ||||||
ASV142 | Genus: Cryptococcus | 572 | 39 | 116 | 19 | ||||||
ASV145 | Taphrina tormentillae | 747 | 33 | 94 | 19 | ||||||
ASV149 | Dioszegia rishiriensis | 686 | 40 | 132 | 19 | ||||||
ASV158 | Vishniacozyma victoriae | 669 | 26 | 42 | 6 | ||||||
ASV160 | Order: Hypocreales | 110 | 27 | 548 | 38 | ||||||
ASV169 | Order: Erythrobasidiales | 490 | 34 | 121 | 21 | ||||||
ASV178 | Genus: Dioszegia | 902 | 38 | 17 | 5 | ||||||
ASV195 | Filobasidium magnum | 520 | 32 | 89 | 17 | ||||||
ASV196 | Zymoseptoria verkleyi | 54 | 18 | 342 | 32 | ||||||
ASV197 | Class: Cystobasidiomycetes | 385 | 34 | 84 | 12 | ||||||
ASV227 | Genus: Limonomyces | 213 | 7 | 0 | 0 | 135 | 6 | ||||
ASV234 | Filobasidium stepposum | 514 | 28 | 18 | 10 | ||||||
ASV237 | Papiliotrema frias | 485 | 32 | 32 | 12 | ||||||
ASV249 | Class: Lecanoromycetes | 100 | 6 | 77 | 5 | 0 | 0 | ||||
ASV260 | Genus: Filobasidium | 282 | 29 | 63 | 12 | ||||||
ASV272 | Kingdom: Fungi | 168 | 28 | 34 | 13 | ||||||
ASV273 | Filobasidium oeirense | 245 | 26 | 9 | 4 | ||||||
ASV281 | Genus: Phaeosphaeria | 49 | 10 | 193 | 28 | ||||||
ASV283 | Protomyces inouyei | 324 | 24 | 0 | 0 | ||||||
ASV288 | Order: Holtermanniales | 283 | 28 | 38 | 6 | ||||||
ASV289 | Dioszegia rishiriensis | 151 | 18 | 18 | 4 | ||||||
ASV298 | Genus: Parastagonospora | 29 | 4 | 181 | 21 | ||||||
ASV301 | Filobasidium wieringae | 259 | 29 | 15 | 5 | ||||||
ASV318 | Sporobolomyces roseus | 179 | 28 | 1 | 2 | ||||||
ASV323 | Order: Microstromatales | 142 | 22 | 30 | 2 | ||||||
ASV367 | Order: Pleosporales | 18 | 3 | 117 | 20 | ||||||
ASV387 | Genus: Phaeosphaeria | 21 | 4 | 94 | 17 | ||||||
ASV533 | Family: Extremaceae | 33 | 8 | 6 | 3 | 0 | 0 | ||||
ASV552 | Apenidiella strumelloidea | 3 | 2 | 40 | 13 | ||||||
ASV837 | Phylum: Ascomycota | 6 | 6 | 7 | 4 | 0 | 0 | ||||
ASV875 | Phylum: Ascomycota | 13 | 8 | 0 | 0 | 0 | 3 |
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Dale, J.C.M.; Newman, J.A. A First Draft of the Core Fungal Microbiome of Schedonorus arundinaceus with and without Its Fungal Mutualist Epichloë coenophiala. J. Fungi 2022, 8, 1026. https://doi.org/10.3390/jof8101026
Dale JCM, Newman JA. A First Draft of the Core Fungal Microbiome of Schedonorus arundinaceus with and without Its Fungal Mutualist Epichloë coenophiala. Journal of Fungi. 2022; 8(10):1026. https://doi.org/10.3390/jof8101026
Chicago/Turabian StyleDale, Jenna C. M., and Jonathan A. Newman. 2022. "A First Draft of the Core Fungal Microbiome of Schedonorus arundinaceus with and without Its Fungal Mutualist Epichloë coenophiala" Journal of Fungi 8, no. 10: 1026. https://doi.org/10.3390/jof8101026