Functional Analysis and Genome Mining Reveal High Potential of Biocontrol and Plant Growth Promotion in Nodule-Inhabiting Bacteria Within Paenibacillus polymyxa Complex.

Md Arshad Ali,Bin Li,Xuqing Li,Yanni Yin,Ting Xie,Yang Lou,Rahila Hafeez,Afsana Hossain,Li Lin,Qianli An,Jianli Yan

doi:10.3389/fmicb.2020.618601

Abstract

Bacteria belonging to the genus Paenibacillus were frequently isolated from legume nodules. The nodule-inhabiting Paenibacillus as a resource of biocontrol and plant growth-promoting endophytes has rarely been explored. This study explored the nodule-inhabiting Paenibacillus’ antifungal activities and biocontrol potentials against broad-spectrum important phytopathogenic fungi. We collected strains which were isolated from nodules of Robinia pseudoacacia, Dendrolobium triangulare, Ormosia semicastrata, Cicer arietinum, Acacia crassicarpa, or Acacia implexa and belong to P. peoriae, P. kribbensis, P. endophyticus, P. enshidis, P. puldeungensis, P. taichungensis, or closely related to P. kribbensis, or P. anseongense. These nodule-inhabiting Paenibacillus showed diverse antagonistic activities against five phytopathogenic fungi (Fusarium graminearum, Magnaporthe oryzae, Rhizoctonia solani, Sclerotinia sclerotiorum, and Botrytis cinerea). Six strains within the P. polymyxa complex showed broad-spectrum and potent activities against all the five pathogens, and produced multiple hydrolytic enzymes, siderophores, and lipopeptide fusaricidins. Fusaricidins are likely the key antimicrobials responsible for the broad-spectrum antifungal activities. The nodule-inhabiting strains within the P. polymyxa complex were able to epiphytically and endophytically colonize the non-host wheat plants, produce indole acetic acids (IAA), and dissolve calcium phosphate and calcium phytate. P. peoriae strains RP20, RP51, and RP62 could fix N2. P. peoriae RP51 and Paenibacillus sp. RP31, which showed potent plant colonization and plant growth-promotion competence, effectively control fungal infection in planta. Genome mining revealed that all strains (n = 76) within the P. polymyxa complex contain ipdC gene encoding indole-3-pyruvate decarboxylase for biosynthesis of IAA, 96% (n = 73) contain the fus cluster for biosynthesis of fusaricidins, and 43% (n = 33) contain the nif cluster for nitrogen fixation. Together, our study highlights that endophytic strains within the P. polymyxa complex have a high probability to be effective biocontrol agents and biofertilizers and we propose an effective approach to screen strains within the P. polymyxa complex.

Highlights

The intense use of agrochemicals including chemical pesticides, synthetic fertilizers, and plant growth regulators to increase crop yields to meet the increasing food demand for increasing population has intensified the side effects of agrochemicals on agriculture, human health, and ecosystems (Lamichhane et al, 2016; Carvalho, 2017)
Strains RP20, RP51, and RP62 isolated from nodules of Robinia pseudoacacia and strain CFCC 1854 isolated from Dendrolobium triangulare were classified to P. peoriae because their 16S rRNA gene sequences and that of P. peoriae type strain have identities above 99.6% and phylogenetically grouped together (Figure 1)
Strain CFCC 1865 isolated from nodules of Ormosia semicastrata was classified to P. kribbensis because its 16S rRNA gene sequence and that of P. kribbensis type strain AM49T have an identity of 99.7% and phylogenetically grouped together

Summary

Introduction

The intense use of agrochemicals including chemical pesticides, synthetic fertilizers, and plant growth regulators to increase crop yields to meet the increasing food demand for increasing population has intensified the side effects of agrochemicals on agriculture, human health, and ecosystems (Lamichhane et al, 2016; Carvalho, 2017). The microbe-based biological control agents and biofertilizers are ecofriendly alternatives to control plant diseases and promote crop growth and are growingly developed to reduce the use of agrochemicals and support the sustainable agriculture (Grady et al, 2016; Alori et al, 2017; Cassán et al, 2020). Like endospore-forming Bacillus, easy mass production in liquid culture, easy formulation, and long shelf-life support Paenibacillus to be promising biocontrol agents and biofertilizers (McSpadden Gardener, 2004; Grady et al, 2016; Rybakova et al, 2016)

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Conclusion