Culminating in the 1950’s, bananas, the world’s most extensive perennial monoculture, suffered one of the most devastating disease epidemics in history. In Latin America and the Caribbean, Fusarium wilt (FW) caused by the soil-borne fungus Fusarium oxysporum f. sp. cubense (FOC), forced the abandonment of the Gros Michel-based export banana industry. Comparative microbiome analyses performed between healthy and diseased Gros Michel plants on FW-infested farms in Nicaragua and Costa Rica revealed significant shifts in the gammaproteobacterial microbiome. Although we found substantial differences in the banana microbiome between both countries and a higher impact of FOC on farms in Costa Rica than in Nicaragua, the composition especially in the endophytic microhabitats was similar and the general microbiome response to FW followed similar rules. Gammaproteobacterial diversity and community members were identified as potential health indicators. Healthy plants revealed an increase in potentially plant-beneficial Pseudomonas and Stenotrophomonas, while diseased plants showed a preferential occurrence of Enterobacteriaceae known for their plant-degrading capacity. Significantly higher microbial rhizosphere diversity found in healthy plants could be indicative of pathogen suppression events preventing or minimizing disease expression. This first study examining banana microbiome shifts caused by FW under natural field conditions opens new perspectives for its biological control.

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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.

The root-knot nematode, Meloidogyne incognita, is among the most damaging agricultural pests, particularly to tomato. The mutualistic endophytes Fusarium oxysporum strain Fo162 (Fo162) and Rhizobium etli strain G12 (G12) have been shown to systemically induce resistance toward M. incognita. By using triple-split-root tomato plants, spatially separated but simultaneous inoculation of both endophytes did not lead to additive reductions in M. incognita infection. More importantly, spatially separated inoculation of Fo162 and G12 led to a reduction in Fo162 root colonization of 35 and 39% when G12 was inoculated on a separate root section of the same plant in two independent experiments. In an additional split-root experiment, spatial separation of Fo162 and G12 resulted in a reduction of Fo162 root colonization of approximately 50% over the water controls in two independent experiments. The results suggested that the suppressive activity of G12 on Fo162 and M. incognita is possibly related to the induction of specific plant defense mechanisms. Thus, although Fo162 and G12 have the ability to systemically repress M. incognita infection in tomato, they can be considered incompatible biocontrol agents when both organisms are present simultaneously on the same root system.