Agroforestry leads to shifts within the gammaproteobacterial microbiome of banana plants cultivated in Central America

Abstract

Bananas (Musa spp.) belong to the most important global food commodities, and their cultivation represents the world's largest monoculture. Although the plant-associated microbiome has substantial influence on plant growth and health, there is a lack of knowledge of the banana microbiome and its influencing factors. We studied the impact of (i) biogeography, and (ii) agroforestry on the banana-associated gammaproteobacterial microbiome analyzing plants grown in smallholder farms in Nicaragua and Costa Rica. Profiles of 16S rRNA genes revealed high abundances of Pseudomonadales, Enterobacteriales, Xanthomonadales, and Legionellales. An extraordinary high diversity of the gammaproteobacterial microbiota was observed within the endophytic microenvironments (endorhiza and pseudostem), which was similar in both countries. Enterobacteria were identified as dominant group of above-ground plant parts (pseudostem and leaves). Neither biogeography nor agroforestry showed a statistically significant impact on the gammaproteobacterial banana microbiome in general. However, indicator species for each microenvironment and country, as well as for plants grown in Coffea intercropping systems with and without agri-silvicultural production of different Fabaceae trees (Inga spp. in Nicaragua and Erythrina poeppigiana in Costa Rica) could be identified. For example, banana plants grown in agroforestry systems were characterized by an increase of potential plant-beneficial bacteria, like Pseudomonas and Stenotrophomonas, and on the other side by a decrease of Erwinia. Hence, this study could show that as a result of legume-based agroforestry the indigenous banana-associated gammaproteobacterial community noticeably shifted.

Members of Gammaproteobacteria as indicator species of healthy banana plants on Fusarium wilt-infested fields in Central America

“…In this scenario, banana and soil microbiota are hypothesized to play an important role1314 as already shown in other agricultural systems1516. Recently, we showed that AFS lead to shifts within the gammaproteobacterial microbiome of banana plants cultivated in Central America917. Gammaproteobacteria have been identified as crucial part within other plant microbiomes1819.…”

“…The taxonomic composition of the gammaproteobacterial banana microbiome inhabiting the individual microenvironments of healthy Gros Michel plants cultivated in Nicaragua and Costa Rica was analyzed in detail in our previous study comparing different agroforestry conditions9. In the present study encompassing samples from healthy and FW-infested plants, nearly all quality sequences could be assigned below the class level.…”

“…For example, comparative analyses between infested and healthy plants revealed unclassified plant-associated species of Stenotrophomonas and Pseudomonas as potential health indicators, which can be used as biological control agents. These two gammaproteobacterial genera were also found in increased abundances in the microbiome of Gros Michel bananas grown under legume-based agroforestry conditions, where a lower FW incidence was noted in comparison to banana monocultures917. Both genera are known to comprise some plant-beneficial species: For example, the species Stenotrophomonas rhizophila has become a model bacterium for a rhizosphere- and phylloplane-competent, salt- tolerant plant growth promoter and stress protecting agent35363738.…”

“…At the time of sampling, each site had been under shaded coffee production for at least 30 years. The exact locations of the farms are given in Köberl et al 9,. where the impact of agroforestry was investigated.…”

“…Even with expansion of Cavendish varieties, millions smallholders in LAC continued depending on FOC R1-susceptible varieties, which are preferred on local markets. Aiming to reduce the FW impact, some of these varieties are grown in agroforestry systems (AFS), mainly associated with Coffea and Fabaceae trees9. Although FW epidemics in AFS might be generally lower compared with intensive monocultures, farmers still face the impact of the disease, which often limits both expansion and increased farmer’s income.…”