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Bacterial communities associated with anthracnose symptomatic and asymptomatic leaves of guarana, an endogenous tropical crop, and their pathogen antagonistic effects

Abstract

Plants are colonized by diverse microorganisms that can substantially impact their health and growth. Understanding bacterial diversity and the relationships between bacteria and phytopathogens may be key to finding effective biocontrol agents. We evaluated the bacterial community associated with anthracnose symptomatic and asymptomatic leaves of guarana, a typical tropical crop. Bacterial communities were assessed through culture-independent techniques based on extensive 16S rRNA sequencing, and cultured bacterial strains were evaluated for their ability to inhibit the growth of Colletotrichum sp. as well as for enzyme and siderophore production. The culture-independent method revealed that Proteobacteria was the most abundant phylum, but many sequences were unclassified. The emergence of anthracnose disease did not significantly affect the bacterial community, but the abundance of the genera Acinetobacter, Pseudomonas and Klebsiella were significantly higher in the symptomatic leaves. In vitro growth of Colletotrichum sp. was inhibited by 11.38% of the cultured bacterial strains, and bacteria with the highest inhibition rates were isolated from symptomatic leaves, while asymptomatic leaves hosted significantly more bacteria that produced amylase and polygalacturonase. The bacterial isolate Bacillus sp. EpD2-5 demonstrated the highest inhibition rate against Colletotrichum sp., whereas the isolates EpD2-12 and FD5-12 from the same genus also had high inhibition rates. These isolates were also able to produce several hydrolytic enzymes and siderophores, indicating that they may be good candidates for the biocontrol of anthracnose. Our work demonstrated the importance of using a polyphasic approach to study microbial communities from plant diseases, and future work should focus on elucidating the roles of culture-independent bacterial communities in guarana anthracnose disease.

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Acknowledgements

We are thankful to Joelma Marcon and Jose Antônio da Silva for performing the biological sampling and support with the experiments. This work was supported by grants from the São Paulo Research Foundation FAPESP (Grant number 2009/53376-2, 2010/14382-4) in association with the Amazon Research Foundation (FAPEAM). We would like to thank FAPESP for the fellowship to Maria Leticia Bonatelli (Grant number 2010/14382-4), Sarina Tsui (Grant number 2010/15192-4) and Bruna Durante Batista (Grant number 2011/05204-8). We also thank the National Council for Scientific and Technological Development (CNPq) for the fellowship to Manuella Nóbrega Dourado (Grant number 150228/2017-1).

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Correspondence to Maria Carolina Quecine.

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Communicated by Erko Stackebrandt.

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Bonatelli, M.L., Tsui, S., Batista, B.D. et al. Bacterial communities associated with anthracnose symptomatic and asymptomatic leaves of guarana, an endogenous tropical crop, and their pathogen antagonistic effects. Arch Microbiol 201, 1061–1073 (2019). https://doi.org/10.1007/s00203-019-01677-1

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  • DOI: https://doi.org/10.1007/s00203-019-01677-1

Keywords

  • Bacterial community
  • Paullinia cupana
  • Colletotrichum sp.
  • Amazon rainforest
  • Biological control
  • Enzymes