Spatio-Temporal Variation in the Phyllospheric Microbial Biodiversity of Alternaria Alternata-Infected Tobacco Foliage

Phyllospheric microbial composition of tobacco (Nicotiana tabacum L.) is contingent upon certain factors, such as the growth stage of the plant, leaf position, and cultivar and its geographical location, which influence, either directly or indirectly, the growth, overall health, and production of th...

Full description

Bibliographic Details
Main Authors: Yuan-feng Dai, Xiao-mao Wu, Han-cheng Wang, Wen-hong Li, Liu-ti Cai, Ji-xin Li, Feng Wang, Shafaque Sehar, Imran Haider Shamsi
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.920109/full
_version_ 1828777732272553984
author Yuan-feng Dai
Yuan-feng Dai
Yuan-feng Dai
Xiao-mao Wu
Han-cheng Wang
Wen-hong Li
Liu-ti Cai
Ji-xin Li
Feng Wang
Shafaque Sehar
Imran Haider Shamsi
author_facet Yuan-feng Dai
Yuan-feng Dai
Yuan-feng Dai
Xiao-mao Wu
Han-cheng Wang
Wen-hong Li
Liu-ti Cai
Ji-xin Li
Feng Wang
Shafaque Sehar
Imran Haider Shamsi
author_sort Yuan-feng Dai
collection DOAJ
description Phyllospheric microbial composition of tobacco (Nicotiana tabacum L.) is contingent upon certain factors, such as the growth stage of the plant, leaf position, and cultivar and its geographical location, which influence, either directly or indirectly, the growth, overall health, and production of the tobacco plant. To better understand the spatiotemporal variation of the community and the divergence of phyllospheric microflora, procured from healthy and diseased tobacco leaves infected by Alternaria alternata, the current study employed microbe culturing, high-throughput technique, and BIOLOG ECO. Microbe culturing resulted in the isolation of 153 culturable fungal isolates belonging to 33 genera and 99 bacterial isolates belonging to 15 genera. High-throughput sequencing revealed that the phyllosphere of tobacco was dominantly colonized by Ascomycota and Proteobacteria, whereas, the most abundant fungal and bacterial genera were Alternaria and Pseudomonas. The relative abundance of Alternaria increased in the upper and middle healthy groups from the first collection time to the third, whereas, the relative abundance of Pseudomonas, Sphingomonas, and Methylobacterium from the same positions increased during gradual leaf aging. Non-metric multi-dimensional scaling (NMDs) showed clustering of fungal communities in healthy samples, while bacterial communities of all diseased and healthy groups were found scattered. FUNGuild analysis, from the first collection stage to the third one in both groups, indicated an increase in the relative abundance of Pathotroph-Saprotroph, Pathotroph-Saprotroph-Symbiotroph, and Pathotroph-Symbiotroph. Inclusive of all samples, as per the PICRUSt analysis, the predominant pathway was metabolism function accounting for 50.03%. The average values of omnilog units (OUs) showed relatively higher utilization rates of carbon sources by the microbial flora of healthy leaves. According to the analysis of genus abundances, leaf growth and leaf position were the important drivers of change in structuring the microbial communities. The current findings revealed the complex ecological dynamics that occur in the phyllospheric microbial communities over the course of a spatiotemporal varying environment with the development of tobacco brown spots, highlighting the importance of community succession.
first_indexed 2024-12-11T16:28:04Z
format Article
id doaj.art-a7177912f26647f594de56ab0437c6d9
institution Directory Open Access Journal
issn 1664-302X
language English
last_indexed 2024-12-11T16:28:04Z
publishDate 2022-07-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj.art-a7177912f26647f594de56ab0437c6d92022-12-22T00:58:40ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-07-011310.3389/fmicb.2022.920109920109Spatio-Temporal Variation in the Phyllospheric Microbial Biodiversity of Alternaria Alternata-Infected Tobacco FoliageYuan-feng Dai0Yuan-feng Dai1Yuan-feng Dai2Xiao-mao Wu3Han-cheng Wang4Wen-hong Li5Liu-ti Cai6Ji-xin Li7Feng Wang8Shafaque Sehar9Imran Haider Shamsi10Department of Plant Protection, Institute of Crop Protection, College of Agriculture, Guizhou University, Guiyang, ChinaGuizhou Provincial Academician Workstation of Microbiology and Health, Guizhou Academy of Tobacco Science, Guiyang, ChinaBijie Tobacco Company, Bijie, ChinaDepartment of Plant Protection, Institute of Crop Protection, College of Agriculture, Guizhou University, Guiyang, ChinaGuizhou Provincial Academician Workstation of Microbiology and Health, Guizhou Academy of Tobacco Science, Guiyang, ChinaGuizhou Institute of Plant Protection, Guizhou Academy of Agricultural Sciences, Guiyang, ChinaGuizhou Provincial Academician Workstation of Microbiology and Health, Guizhou Academy of Tobacco Science, Guiyang, ChinaGuizhou Tobacco Company of CNTC, China National Tobacco Corporation, Guiyang, ChinaGuizhou Provincial Academician Workstation of Microbiology and Health, Guizhou Academy of Tobacco Science, Guiyang, ChinaZhejiang Key Laboratory of Crop Germplasm Resource, Department of Agronomy, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, ChinaZhejiang Key Laboratory of Crop Germplasm Resource, Department of Agronomy, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, ChinaPhyllospheric microbial composition of tobacco (Nicotiana tabacum L.) is contingent upon certain factors, such as the growth stage of the plant, leaf position, and cultivar and its geographical location, which influence, either directly or indirectly, the growth, overall health, and production of the tobacco plant. To better understand the spatiotemporal variation of the community and the divergence of phyllospheric microflora, procured from healthy and diseased tobacco leaves infected by Alternaria alternata, the current study employed microbe culturing, high-throughput technique, and BIOLOG ECO. Microbe culturing resulted in the isolation of 153 culturable fungal isolates belonging to 33 genera and 99 bacterial isolates belonging to 15 genera. High-throughput sequencing revealed that the phyllosphere of tobacco was dominantly colonized by Ascomycota and Proteobacteria, whereas, the most abundant fungal and bacterial genera were Alternaria and Pseudomonas. The relative abundance of Alternaria increased in the upper and middle healthy groups from the first collection time to the third, whereas, the relative abundance of Pseudomonas, Sphingomonas, and Methylobacterium from the same positions increased during gradual leaf aging. Non-metric multi-dimensional scaling (NMDs) showed clustering of fungal communities in healthy samples, while bacterial communities of all diseased and healthy groups were found scattered. FUNGuild analysis, from the first collection stage to the third one in both groups, indicated an increase in the relative abundance of Pathotroph-Saprotroph, Pathotroph-Saprotroph-Symbiotroph, and Pathotroph-Symbiotroph. Inclusive of all samples, as per the PICRUSt analysis, the predominant pathway was metabolism function accounting for 50.03%. The average values of omnilog units (OUs) showed relatively higher utilization rates of carbon sources by the microbial flora of healthy leaves. According to the analysis of genus abundances, leaf growth and leaf position were the important drivers of change in structuring the microbial communities. The current findings revealed the complex ecological dynamics that occur in the phyllospheric microbial communities over the course of a spatiotemporal varying environment with the development of tobacco brown spots, highlighting the importance of community succession.https://www.frontiersin.org/articles/10.3389/fmicb.2022.920109/fullmicrobial communityAlternaria alternatatobacco brown spothigh-throughput sequencingmicrobial functional diversitybiolog-eco
spellingShingle Yuan-feng Dai
Yuan-feng Dai
Yuan-feng Dai
Xiao-mao Wu
Han-cheng Wang
Wen-hong Li
Liu-ti Cai
Ji-xin Li
Feng Wang
Shafaque Sehar
Imran Haider Shamsi
Spatio-Temporal Variation in the Phyllospheric Microbial Biodiversity of Alternaria Alternata-Infected Tobacco Foliage
Frontiers in Microbiology
microbial community
Alternaria alternata
tobacco brown spot
high-throughput sequencing
microbial functional diversity
biolog-eco
title Spatio-Temporal Variation in the Phyllospheric Microbial Biodiversity of Alternaria Alternata-Infected Tobacco Foliage
title_full Spatio-Temporal Variation in the Phyllospheric Microbial Biodiversity of Alternaria Alternata-Infected Tobacco Foliage
title_fullStr Spatio-Temporal Variation in the Phyllospheric Microbial Biodiversity of Alternaria Alternata-Infected Tobacco Foliage
title_full_unstemmed Spatio-Temporal Variation in the Phyllospheric Microbial Biodiversity of Alternaria Alternata-Infected Tobacco Foliage
title_short Spatio-Temporal Variation in the Phyllospheric Microbial Biodiversity of Alternaria Alternata-Infected Tobacco Foliage
title_sort spatio temporal variation in the phyllospheric microbial biodiversity of alternaria alternata infected tobacco foliage
topic microbial community
Alternaria alternata
tobacco brown spot
high-throughput sequencing
microbial functional diversity
biolog-eco
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.920109/full
work_keys_str_mv AT yuanfengdai spatiotemporalvariationinthephyllosphericmicrobialbiodiversityofalternariaalternatainfectedtobaccofoliage
AT yuanfengdai spatiotemporalvariationinthephyllosphericmicrobialbiodiversityofalternariaalternatainfectedtobaccofoliage
AT yuanfengdai spatiotemporalvariationinthephyllosphericmicrobialbiodiversityofalternariaalternatainfectedtobaccofoliage
AT xiaomaowu spatiotemporalvariationinthephyllosphericmicrobialbiodiversityofalternariaalternatainfectedtobaccofoliage
AT hanchengwang spatiotemporalvariationinthephyllosphericmicrobialbiodiversityofalternariaalternatainfectedtobaccofoliage
AT wenhongli spatiotemporalvariationinthephyllosphericmicrobialbiodiversityofalternariaalternatainfectedtobaccofoliage
AT liuticai spatiotemporalvariationinthephyllosphericmicrobialbiodiversityofalternariaalternatainfectedtobaccofoliage
AT jixinli spatiotemporalvariationinthephyllosphericmicrobialbiodiversityofalternariaalternatainfectedtobaccofoliage
AT fengwang spatiotemporalvariationinthephyllosphericmicrobialbiodiversityofalternariaalternatainfectedtobaccofoliage
AT shafaquesehar spatiotemporalvariationinthephyllosphericmicrobialbiodiversityofalternariaalternatainfectedtobaccofoliage
AT imranhaidershamsi spatiotemporalvariationinthephyllosphericmicrobialbiodiversityofalternariaalternatainfectedtobaccofoliage