Metagenomic and Metatranscriptomic Analyses of Diverse Watermelon Cultivars Reveal the Role of Fruit Associated Microbiome in Carbohydrate Metabolism and Ripening of Mature Fruits.

Thangasamy Saminathan,Carlos Lopez,Marleny García,Venkata L Abburi,Amnon Levi,Nagamani Balagurusamy,Umesh K Reddy,Padma Nimmakayala,Abiodun Bodunrin,Bandana Ghimire

doi:10.3389/fpls.2018.00004

Abstract

The plant microbiome is a key determinant of plant health and productivity, and changes in the plant microbiome can alter the tolerance to biotic and abiotic stresses and the quality of end produce. Little is known about the microbial diversity and its effect on carbohydrate metabolism in ripe fruits. In this study, we aimed to understand the diversity and function of microorganisms in relation to carbohydrate metabolism of ripe watermelon fruits. We used 16S metagenomics and RNAseq metatranscriptomics for analysis of red (PI459074, Congo, and SDRose) and yellow fruit-flesh cultivars (PI227202, PI435990, and JBush) of geographically and metabolically diverse watermelon cultivars. Metagenomics data showed that Proteobacteria were abundant in SDRose and PI227202, whereas Cyanobacteria were most abundant in Congo and PI4559074. In the case of metatranscriptome data, Proteobacteria was the most abundant in all cultivars. High expression of genes linked to infectious diseases and the expression of peptidoglycan hydrolases associated to pathogenicity of eukaryotic hosts was observed in SDRose, which could have resulted in low microbial diversity in this cultivar. The presence of GH28, associated with polygalacturonase activity in JBush and SDRose could be related to cell wall modifications including de-esterification and depolymerization, and consequent loss of galacturonic acid and neutral sugars. Moreover, based on the KEGG annotation of the expressed genes, nine α-galactosidase genes involved in key processes of galactosyl oligosaccharide metabolism, such as raffinose family were identified and galactose metabolism pathway was reconstructed. Results of this study underline the links between the host and fruit-associated microbiome in carbohydrate metabolism of the ripe fruits. The cultivar difference in watermelon reflects the quantum and diversity of the microbiome, which would benefit watermelon and other plant breeders aiming at the holobiont concept to incorporate associated microbiomes in breeding programs.

Highlights

Watermelon (Citrullus lanatus) is a major cucurbit crop grown in tropical and subtropical regions of the world (Chomicki and Renner, 2015)
Ripe fruits were selected based on the following observations: (a) appearance of yellow color of the fruit in the spot touching the ground; (b) the presence of a dried-up stalk attached to the fruit; (c) slightly rough, ridged, and a dull-opaque appearance of rind; and (d) giving a hollow sound when you thump it with your knuckles
The external surface of the watermelon was rinsed with running water, dried and surface-sterilized with 70% ethanol to avoid the interference of epiphytic bacteria contamination

Summary

Introduction

Watermelon (Citrullus lanatus) is a major cucurbit crop grown in tropical and subtropical regions of the world (Chomicki and Renner, 2015). Some microorganisms are able to move systemically within the plant (Hallmann and Berg, 2006; Rosenblueth and MartínezRomero, 2006), whereas others are restricted to below-ground parts of plants (Hallman et al, 2001; Compant et al, 2011). This plant-associated microbiome is highly diverse and comprises a range of different taxa (James et al, 1994; Rosenblueth and Martínez-Romero, 2006). Distinct microbial communities in low density have been reported in flowers, seeds, and fruits (Compant et al, 2010)

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Results