Enterobacter cloacae, an Endophyte That Establishes a Nutrient-Transfer Symbiosis With Banana Plants and Protects Against the Black Sigatoka Pathogen

Author(s):Show less -

Macedo-Raygoza, Gloria M. ^{[1, 2]} ; Valdez-Salas, Benjamin ^[1] ; Prado, Fernanda M. ^[3] ; Prieto, Katia R. ^{[3, 4]} ; Yamaguchi, Lydia F. ^[5] ; Kato, Massuo J. ^[5] ; Canto-Canche, Blondy B. ^[6] ; Carrillo-Beltran, Monica ^[1] ; Di Mascio, Paolo ^[3] ; White, James F. ^[7] ; Beltran-Garcia, Miguel J. ^[2]

Affiliation

^[1] Univ Autonoma Baja California, Engn Inst, Mexicali - Mexico

^[2] Univ Autonoma Guadalajara, Dept Chem, Zapopan - Mexico

^[3] Univ Sao Paulo, Inst Chem, Dept Biochem, Sao Paulo - Brazil

^[4] Univ Franca, PPG Ciencia Anim, Franca - Brazil

^[5] Univ Sao Paulo, Dept Fundamental Chem, Inst Chem, Sao Paulo - Brazil

^[6] Ctr Invest Cient Yucatan AC, Biotechnol Unit, Merida - Mexico

^[7] Rutgers State Univ, Sch Environm & Biol Sci, Dept Plant Biol, New Brunswick, NJ - USA

• Document type: Journal article
• Source: FRONTIERS IN MICROBIOLOGY; v. 10, MAY 7 2019.
• Web of Science Citations: 0

Abstract

Banana (Musa spp.) is an important crop worldwide, but black Sigatoka disease caused by the fungus Pseudocercospora fijiensis threatens fruit production. In this work, we examined the potential of the endophytes of banana plants Enterobacter cloacae and Klebsiella pneumoniae, as antagonists of P fijiensis and support plant growth in nutrient limited soils by N-transfer. The two bacterial isolates were identified by MALDI-TOF mass spectrometry and corroborated by 16S rRNA sequence analysis. Both bacteria were positive for beneficial traits such as N-fixation, indole acetic acid production, phosphate solubilization, negative for 1-aminocyclopropane 1-carboxylic acid deaminase and were antagonistic to P fijiensis. To measure the effects on plant growth, the two plant bacteria and an E. coil strain (as non-endophyte), were inoculated weekly for 60 days as active cells (AC) and heat-killed cells (HKC) into plant microcosms without nutrients and compared to a water only treatment, and a mineral nutrients solution (MMN) treatment. Bacterial treatments increased growth parameters and prevented accelerated senescence, which was observed for water and mineral nutrients solution (MMN) treatments used as controls. Plants died after the first 20 days of being irrigated with water; irrigation with MMN enabled plants to develop some new leaves, but plants lost weight (-30%) during the same period. Plants treated with bacteria showed good growth, but E. cloacae AC treated plants had significantly greater biomass than the E. cloacae HKC. After 60 days, plants inoculated with E. cloacae AC showed intracellular bacteria within root cells, suggesting that a stable symbiosis was established. To evaluate the transference of organic N from bacteria into the plants, the 3 bacteria were grown with (NH4Cl)-N-15 or (NaNO3)-N-15 as the nitrogen source. The( 15)N transferred from bacteria to plant tissues was measured by pheophytin isotopomer abundance. The relative abundance of the isotopomers m/z 872.57, 873.57, 874.57, 875.57, 876.57 unequivocally demonstrated that plants acquired N-15 atoms directly from bacterial cells, using them as a source of N, to support plant growth in restricted nutrient soils. E. cloacae might be a new alternative to promote growth and health of banana crops. (AU)

• FAPESP's process: 12/12663-1 - Singlet molecular oxygen and peroxides in chemical biology
• Grantee: Paolo Di Mascio
• Support Opportunities: Research Projects - Thematic Grants
• FAPESP's process: 13/07937-8 - Redoxome - Redox Processes in Biomedicine
• Grantee: Ohara Augusto
• Support Opportunities: Research Grants - Research, Innovation and Dissemination Centers - RIDC
• FAPESP's process: 14/50316-7 - Dimensions US-Biota São Paulo: Chemically mediated multi-trophic interaction diversity across tropical gradients
• Grantee: Massuo Jorge Kato
• Support Opportunities: BIOTA-FAPESP Program - Thematic Grants