Foliar Mycobiome Remains Unaltered Under Urban Air-pollution but Differentially Express Stress-related Genes

Overview

Journal Microb Ecol

Specialties Environmental Health
Microbiology

Date 2024 May 16

PMID 38755460

Authors

Valeria Stephany Flores-Almaraz

Camille Truong

Diana Hernandez-Oaxaca

Veronica Reyes-Galindo

Alicia Mastretta-Yanes

Juan Pablo Jaramillo-Correa

Rodolfo Salas-Lizana

Affiliations

Soon will be listed here.

Abstract

Air pollution caused by tropospheric ozone contributes to the decline of forest ecosystems; for instance, sacred fir, Abies religiosa (Kunth) Schltdl. & Cham. forests in the peri-urban region of Mexico City. Individual trees within these forests exhibit variation in their response to ozone exposure, including the severity of visible symptoms in needles. Using RNA-Seq metatranscriptomic data and ITS2 metabarcoding, we investigated whether symptom variation correlates with the taxonomic and functional composition of fungal mycobiomes from needles collected in this highly polluted area in the surroundings of Mexico City. Our findings indicate that ozone-related symptoms do not significantly correlate with changes in the taxonomic composition of fungal mycobiomes. However, genes coding for 30 putative proteins were differentially expressed in the mycobiome of asymptomatic needles, including eight genes previously associated with resistance to oxidative stress. These results suggest that fungal communities likely play a role in mitigating the oxidative burst caused by tropospheric ozone in sacred fir. Our study illustrates the feasibility of using RNA-Seq data, accessible from global sequence repositories, for the characterization of fungal communities associated with plant tissues, including their gene expression.

References

Zuo Y, Li X, Yang J, Liu J, Zhao L, He X . Fungal Endophytic Community and Diversity Associated with Desert Shrubs Driven by Plant Identity and Organ Differentiation in Extremely Arid Desert Ecosystem. J Fungi (Basel). 2021; 7(7). PMC: 8306007. DOI: 10.3390/jof7070578. View

Ansell R, Granath K, Hohmann S, Thevelein J, Adler L . The two isoenzymes for yeast NAD+-dependent glycerol 3-phosphate dehydrogenase encoded by GPD1 and GPD2 have distinct roles in osmoadaptation and redox regulation. EMBO J. 1997; 16(9):2179-87. PMC: 1169820. DOI: 10.1093/emboj/16.9.2179. View

Cho K, Tiwari S, Agrawal S, Torres N, Agrawal M, Sarkar A . Tropospheric ozone and plants: absorption, responses, and consequences. Rev Environ Contam Toxicol. 2011; 212:61-111. DOI: 10.1007/978-1-4419-8453-1_3. View

Wemheuer F, Wemheuer B, Daniel R, Vidal S . Deciphering bacterial and fungal endophyte communities in leaves of two maple trees with green islands. Sci Rep. 2019; 9(1):14183. PMC: 6775154. DOI: 10.1038/s41598-019-50540-2. View

Galperin M, Wolf Y, Makarova K, Vera Alvarez R, Landsman D, Koonin E . COG database update: focus on microbial diversity, model organisms, and widespread pathogens. Nucleic Acids Res. 2020; 49(D1):D274-D281. PMC: 7778934. DOI: 10.1093/nar/gkaa1018. View

Vaghela B, Vashi R, Rajput K, Joshi R . Plant chitinases and their role in plant defense: A comprehensive review. Enzyme Microb Technol. 2022; 159:110055. DOI: 10.1016/j.enzmictec.2022.110055. View

Wangsanut T, Amsri A, Pongpom M . Antibody screening reveals antigenic proteins involved in and human interaction. Front Cell Infect Microbiol. 2023; 13:1118979. PMC: 10315666. DOI: 10.3389/fcimb.2023.1118979. View

Mir A, Park S, Sadat M, Kim S, Choi J, Jeon J . Systematic characterization of the peroxidase gene family provides new insights into fungal pathogenicity in Magnaporthe oryzae. Sci Rep. 2015; 5:11831. PMC: 4488832. DOI: 10.1038/srep11831. View

Menzel P, Ng K, Krogh A . Fast and sensitive taxonomic classification for metagenomics with Kaiju. Nat Commun. 2016; 7:11257. PMC: 4833860. DOI: 10.1038/ncomms11257. View

10.

Reyes-Galindo V, Jaramillo-Correa J, Shishkova S, Sandoval-Zapotitla E, Flores-Ortiz C, Pinero D . Histologic, metabolomic, and transcriptomic differences in fir trees from a peri-urban forest under chronic ozone exposure. Ecol Evol. 2024; 14(5):e11343. PMC: 11091488. DOI: 10.1002/ece3.11343. View

11.

Herranz S, Rodriguez J, Bussink H, Sanchez-Ferrero J, Arst Jr H, Penalva M . Arrestin-related proteins mediate pH signaling in fungi. Proc Natl Acad Sci U S A. 2005; 102(34):12141-6. PMC: 1189327. DOI: 10.1073/pnas.0504776102. View

12.

Bradshaw M, Aime M, Rokas A, Maust A, Moparthi S, Jellings K . Extensive intragenomic variation in the internal transcribed spacer region of fungi. iScience. 2023; 26(8):107317. PMC: 10387565. DOI: 10.1016/j.isci.2023.107317. View

13.

Hohmann S . Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev. 2002; 66(2):300-72. PMC: 120784. DOI: 10.1128/MMBR.66.2.300-372.2002. View

14.

Reyes-Galindo V, Jaramillo-Correa J, Carrasco Nava K, De-la-Rosa-Gonzalez A, Flores Flores D, Martinez M . Evaluating pollution-related damage and restoration success in urban forests with participatory monitoring and digital tools. Conserv Biol. 2023; 37(5):e14112. DOI: 10.1111/cobi.14112. View

15.

Cantalapiedra C, Hernandez-Plaza A, Letunic I, Bork P, Huerta-Cepas J . eggNOG-mapper v2: Functional Annotation, Orthology Assignments, and Domain Prediction at the Metagenomic Scale. Mol Biol Evol. 2021; 38(12):5825-5829. PMC: 8662613. DOI: 10.1093/molbev/msab293. View

16.

Poirier Y, Antonenkov V, Glumoff T, Hiltunen J . Peroxisomal beta-oxidation--a metabolic pathway with multiple functions. Biochim Biophys Acta. 2006; 1763(12):1413-26. DOI: 10.1016/j.bbamcr.2006.08.034. View

17.

Tong S, Wang D, Gao B, Ying S, Feng M . The DUF1996 and WSC domain-containing protein Wsc1I acts as a novel sensor of multiple stress cues in Beauveria bassiana. Cell Microbiol. 2019; 21(12):e13100. DOI: 10.1111/cmi.13100. View

18.

Grabherr M, Haas B, Yassour M, Levin J, Thompson D, Amit I . Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011; 29(7):644-52. PMC: 3571712. DOI: 10.1038/nbt.1883. View

19.

Javed J, Rauf M, Arif M, Hamayun M, Gul H, Ud-Din A . Endophytic Fungal Consortia Enhance Basal Drought-Tolerance in by Upregulating the Antioxidant Enzyme through . Antioxidants (Basel). 2022; 11(9). PMC: 9495891. DOI: 10.3390/antiox11091669. View

20.

Pusztahelyi T, Klement E, Szajli E, Klem J, Miskei M, Karanyi Z . Comparison of transcriptional and translational changes caused by long-term menadione exposure in Aspergillus nidulans. Fungal Genet Biol. 2010; 48(2):92-103. DOI: 10.1016/j.fgb.2010.08.006. View