Responses of the bacterial community of tobacco phyllosphere to summer climate and wildfire disease

Wang, Zhenhua; Fu, Changwu; Tian, Jing; Wei, Wang; Deyuan, Peng; Dai, Xi; Tian, Hanqin; Zhou, Xin; Li, Liangzhi; Yin, Huaqun

doi:10.3389/fpls.2022.1050967

Cited by 5 publications

(11 citation statements)

References 53 publications

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“…This supports the notion that these microorganisms play a crucial role in protecting DNA from damage caused by harmful radiation. These findings are consistent with our previous study, which showed the enrichment of Pseudomonas (LDA = 5.29) and Sphingomonas (LDA = 4.19) during T3, a time period characterized by severe sun exposure ( Wang et al., 2022 ).…”

Section: Resultssupporting

confidence: 93%

Pan-metagenome reveals the abiotic stress resistome of cigar tobacco phyllosphere microbiome

Wang,

Peng,

et al. 2023

Front. Plant Sci.

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The important role of microbial associations in mediating plant protection and responses to abiotic stresses has been widely recognized. However, there have been limited studies on the functional profile of the phyllosphere microbiota from tobacco (Nicotiana tabacum), hindering our understanding of the mechanisms underlying stress resilience in this representative and easy-to-cultivate model species from the solanaceous family. To address this knowledge gap, our study employed shotgun metagenomic sequencing for the first time to analyze the genetic catalog and identify putative plant growth promoting bacteria (PGPB) candidates that confer abiotic stress resilience throughout the growth period of cigar tobacco in the phyllosphere. We identified abundant genes from specific bacterial lineages, particularly Pseudomonas, within the cigar tobacco phyllospheric microbiome. These genes were found to confer resilience against a wide range of stressors, including osmotic and drought stress, heavy metal toxicity, temperature perturbation, organic pollutants, oxidative stress, and UV light damage. In addition, we conducted a virome mining analysis on the metagenome to explore the potential roles of viruses in driving microbial adaptation to environmental stresses. Our results identified a total of 3,320 scaffolds predicted to be viral from the cigar tobacco phyllosphere metagenome, with various phages infecting Pseudomonas, Burkholderia, Enterobacteria, Ralstonia, and related viruses. Within the virome, we also annotated genes associated with abiotic stress resilience, such as alkaline phosphatase D (phoD) for nutrient solubilization and glutamate-5-semialdehyde dehydrogenase (proA) for osmolyte synthesis. These findings shed light on the unexplored roles of viruses in facilitating and transferring abiotic stress resilience in the phyllospheric microbiome through beneficial interactions with their hosts. The findings from this study have important implications for agricultural practices, as they offer potential strategies for harnessing the capabilities of the phyllosphere microbiome to enhance stress tolerance in crop plants.

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Section: Resultssupporting

confidence: 93%

Pan-metagenome reveals the abiotic stress resistome of cigar tobacco phyllosphere microbiome

Wang,

Peng,

et al. 2023

Front. Plant Sci.

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“…Studies of microorganisms in different plant organs or phyllosphere have harbored a “core microbiome.” In our study, core bacterial microbiota during the development of plant belonged to Proteobacteria ( Figure 4 ), with a member of the class Gammaproteobacteria, in which genera Pseudomonas , Acinetobacter , Pantoea , and Enterobacter include. Similar results were reported by Wang et al (2022) . It was reported that these hub members are considered as biocontrol bacteria and have antibiotic activity ( Helfrich et al, 2018 ).…”

Section: Discussionsupporting

confidence: 92%

“…For instance, the squaring stage of tobacco growth is mostly influenced by high rainfall intensity in summer for most subtrobical areas in China. Our results are corroborated with those of Wang et al (2022) , who argued that the enrichment of these genera in summer might be a”cry for help” strategy of plants for the recruitment of microbes in response to biotic and abiotic stresses ( Wang and Song, 2022 ). These heightened levels in diversity and species richness might play part in high functional redundancy within microbiome, and thus could enable it to cope with complex environmental changes and quickly recover from stress.…”

Section: Discussionsupporting

confidence: 89%

“…The tobacco phyllosphere microbiota has recently been studied extensively. For instance, Wang et al (2022) demonstrated the variation of tobacco’s phyllospheric microbial community as a result of the change in summer climatic variables and wildfire disease. The recent study also showed how tobacco leaf’s microorganism communities are affected by local environments ( Hu et al, 2022 ).…”

Section: Introductionmentioning

confidence: 99%

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Microbial composition and diversity of the tobacco leaf phyllosphere during plant development

2023

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Phyllosphere-associated microorganisms affect host plant’s nutrients availability, its growth and ecological functions. Tobacco leaves provide a wide-area habitat for microbial life. Previous studies have mainly focused on phyllosphere microbiota at one time point of tobacco growth process, but more is unknown about dynamic changes in phyllospheric microbial composition from earlier to the late stage of plant development. In the current study, we had determined the bacterial and fungal communities succession of tobacco growth stages (i.e., seedling, squaring, and maturing) by using both 16S rRNA sequencing for bacterial and ITS sequencing for fungi. Our results demonstrated that among tobacco growth stages, the phyllospheric bacterial communities went through more distinct succession than the fungal communities did. Proteobacteria and Actinobacteria exerted the most influence in tobacco development from seedling to squaring stages. At maturing stage, Proteobacteria and Actinobacteria dominance was gradually replaced by Firmicutes and Bacteroidetes. Network analysis revealed that Proteobacteria, as the core phyllospheric microbia, played essential role in stabilizing the whole bacterial network during tobacco development, and consequently rendered it to more profound ecological functions. During tobacco development, the contents of leaf sugar, nicotine, nitrogen and potassium were significantly correlated with either bacterial or fungal communities, and these abiotic factors accounted for 39.3 and 51.5% of the total variation, respectively. We overall evinced that the development of tobacco phyllosphere is accompanied by variant dynamics of phyllospheric microbial community.

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“…Alphaproteobacteria, Sphingobacteria, Clostridia, Gammaproteobacteria and Bacilli were the predominant classes ( Figure 1D ); Enterobacterales, Pseudomonadales, Sphingobacteriales, Clostridiales, Lactobacillales, Rhodospirillales, Alteromonadales, Flavobacteriales, Sphingomonadales, Burkholderiales, and Rhizobiales were the dominant bacterial orders ( Figure 1E ); Finally, Pseudomonas, Stenotrophomonas, Enterobacter, Acinetobacter, Lactococcus, Enterococcus, Clostridium and Sphingobacterium were the dominant bacterial genra ( Figure 1F ). Additionally, the bacterial community structure of cigar tobacco in current study is significantly distinct from that of fine-tuned tobacco that we previously reported ( Wang Z. et al., 2022 ) upon partial least squares-discriminant analysis (PLS-DA), which aligns with the notion that host genotype affect the composition of microbial holobiont ( Supplementary Figure S2 ). The PLS-DA model was validated by a permutation test: R2 intercept = 0.370 and Q2 intercept = -0.402.…”

Section: Resultssupporting

confidence: 82%

Phyllosphere bacterial community dynamics in response to bacterial wildfire disease: succession and interaction patterns

Peng,

Wang,

Tian

et al. 2024

Front. Plant Sci.

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Plants interact with complex microbial communities in which microorganisms play different roles in plant development and health. While certain microorganisms may cause disease, others promote nutrient uptake and resistance to stresses through a variety of mechanisms. Developing plant protection measures requires a deeper comprehension of the factors that influence multitrophic interactions and the organization of phyllospheric communities. High-throughput sequencing was used in this work to investigate the effects of climate variables and bacterial wildfire disease on the bacterial community’s composition and assembly in the phyllosphere of tobacco (Nicotiana tabacum L.). The samples from June (M1), July (M2), August (M3), and September (M4) formed statistically separate clusters. The assembly of the whole bacterial population was mostly influenced by stochastic processes. PICRUSt2 predictions revealed genes enriched in the M3, a period when the plant wildfire disease index reached climax, were associated with the development of the wildfire disease (secretion of virulence factor), the enhanced metabolic capacity and environmental adaption. The M3 and M4 microbial communities have more intricate molecular ecological networks (MENs), bursting with interconnections within a densely networked bacterial population. The relative abundances of plant-beneficial and antagonistic microbes Clostridiales, Bacillales, Lactobacillales, and Sphingobacteriales, showed significant decrease in severally diseased sample (M3) compared to the pre-diseased samples (M1/M2). Following the results of MENs, we further test if the correlating bacterial pairs within the MEN have the possibility to share functional genes and we have unraveled 139 entries of such horizontal gene transfer (HGT) events, highlighting the significance of HGT in shaping the adaptive traits of plant-associated bacteria across the MENs, particularly in relation to host colonization and pathogenicity.

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Responses of the bacterial community of tobacco phyllosphere to summer climate and wildfire disease

Cited by 5 publications

References 53 publications

Pan-metagenome reveals the abiotic stress resistome of cigar tobacco phyllosphere microbiome

Pan-metagenome reveals the abiotic stress resistome of cigar tobacco phyllosphere microbiome

Microbial composition and diversity of the tobacco leaf phyllosphere during plant development

Phyllosphere bacterial community dynamics in response to bacterial wildfire disease: succession and interaction patterns

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