The Bacterial Microbiome of the Tomato Fruit Is Highly Dependent on the Cultivation Approach and Correlates With Flavor Chemistry

Abstract

The modes of interactions between plants and plant-associated microbiota are manifold, and secondary metabolites often play a central role in plant-microbe interactions. Abiotic and biotic (including both plant pathogens and endophytes) stress can affect the composition and concentration of secondary plant metabolites, and thus have an influence on chemical compounds that make up for the taste and aroma of fruit. While the role of microbiota in growth and health of plants is widely acknowledged, relatively little is known about the possible effect of microorganisms on the quality of fruit of plants they are colonizing. In this work, tomato (Solanum lycopersicum L.) plants of five different cultivars were grown in soil and in hydroponics to investigate the impact of the cultivation method on the flavor of fruit, and to assess whether variations in their chemical composition are attributable to shifts in bacterial microbiota. Ripe fruit were harvested and used for bacterial community analysis and for the analysis of tomato volatiles, sugars and acids, all contributing to flavor. Fruit grown in soil showed significantly higher sugar content, whereas tomatoes from plants under hydroponic conditions had significantly higher levels of organic acids. In contrast, aroma profiles of fruit were shaped by the tomato cultivars, rather than the cultivation method. In terms of bacterial communities, the cultivation method significantly defined the community composition in all cultivars, with the bacterial communities in hydroponic tomatoes being more variable that those in tomatoes grown in soil. Bacterial indicator species in soil-grown tomatoes correlated with higher concentrations of volatiles described to be perceived as "green" or "pungent." A soil-grown specific reproducibly occurring ASV (amplicon sequence variants) classified as Bacillus detected solely in "Solarino" tomatoes, which were the sweetest among all cultivars, correlated with the amount of aroma-relevant volatiles as well as of fructose and glucose in the fruit. In contrast, indicator bacterial species in hydroponic-derived tomatoes correlated with aroma compounds with "sweet" and "floral" notes and showed negative correlations with glucose concentrations in fruit. Overall, our results point toward a microbiota-related accumulation of flavor and aroma compounds in tomato fruit, which is strongly dependent on the cultivation substrate and approach.

Keywords: aroma and flavor; bacterial microbiota; hydroponics; organoleptic properties; tomato fruit.

FIGURE 1

Fruit of five tomato cultivars ‘Ardiles,’ ‘Campari,’ ‘Cappricia,’ ‘Savantas’ and ‘Solarino.’ Shown are the mean fresh weight (MFW) and the scoring obtained from a trained tasting panel regarding the level of aroma perception and sugar/acid ratio. Scoring details are listed in Supplementary Table 1.

FIGURE 2

(A) Total concentration of organic volatile compounds (VOCs) in tomato fruit of five different cultivars expressed in mg/L. Letters over each box indicate members of homologous groups according to a Tukey HSD test for pairwise comparisons among tomato cultivars. (B) Principal component analyses (PCA) showing groupings of individual samples colored by tomato cultivar. (C) PCA with individual samples colored according to the employed cultivation method. (D) PCA loadings of VOCs with a contribution >10.

FIGURE 3

(A) Total sugar as well as glucose and fructose concentrations in juices prepared from tomatoes grown in soil and in hydroponics. (B) Sugar concentrations in juices of five different tomato cultivars grown in soil and hydroponics. (C) Total acid as well as malic and citric acid concentrations in juices prepared from tomatoes grown in soil and in hydroponics. (D) Acid concentrations in juices of five different tomato cultivars grown in soil and in hydroponics. Letters over each box indicate members of homologous groups according to a Tukey HSD test for pairwise comparisons among tomato cultivars. Significance values computed by ANOVA for each factor are indicated as (**) for p > 0.01 and (***) for p > 0.001.

FIGURE 4

(A) Total observed rASVs and diversity (Simpsons Index) of tomato fruit grown in soil and in hydroponics. (B) Alpha diversity measures considering the effect of cultivation method in each tomato cultivar. Significance values computed by ANOVA are indicated as (*) for p > 0.05.

FIGURE 5

Variation across samples of both cultivation methods is visible for each tomato cultivar (CAP).

FIGURE 6

(A) Relative abundance of core orders in soil- and hydroponic grown tomato fruit. rASVs represent a higher portion of the overall communities in hydroponic tomatoes (65–82%) as compared to soil derived fruit (∼60%). Reproducibly occurring communities of hydroponic tomatoes lack member rASVs from Flavobacteriales and Kineosporiales. (B) Number of accessory bacterial orders (accessory) that are specific to soil-grown tomatoes or hydroponic-grown fruit. (C) Abundance of 20 predominant accessory bacterial orders detected in tomato fruit. None of these orders were specific to any cultivation method, but rather common among them. (D) Accessory bacterial orders that were specific to each cultivation method occurred in low relative abundance.

FIGURE 7

Relative abundance of 46 indicator rASVs for the Cultivation soil × Cultivar (GxE) interaction correlate with concentrations of at least one aroma or flavor compound in this study. Symbols in cells (+) indicate significant correlations (fdr adjusted p > 0.05). Colors in cells with non-significant correlations have been removed for simplification.