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Title: Metagenomic and metatranscriptomic analysis of the microbiome of watermelon fruits

Author
item SAMINATHAN, THANGASAMY - West Virginia State University
item GARACIA, MARLEENY - West Virginia State University
item GHIMIRE, BANDANA - West Virginia State University
item LOPEZ, CARLOS - West Virginia University
item BODUNRIN, ABIODUN - West Virginia University
item BALAGURUSAMY, NAGAMANI - West Virginia State University
item NIMMAKAYALA, PADMA - West Virginia State University
item HUBER, DAVID - West Virginia State University
item Levi, Amnon
item REDDY, K. UMESH - West Virginia State University

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/3/2018
Publication Date: 1/19/2018
Citation: Saminathan, T., Garacia, M., Ghimire, B., Lopez, C., Bodunrin, A., Balagurusamy, N., Nimmakayala, P., Huber, D., Levi, A., Reddy, K. 2018. Metagenomic and metatranscriptomic analysis of the microbiome of watermelon fruits. Frontiers in Plant Science. 9:1-4. https://doi.org/10.3389/fpls.2018.00004.
DOI: https://doi.org/10.3389/fpls.2018.00004

Interpretive Summary: A wide range of beneficial microorganisms exist in plant tissues. These microorganisms play an important role in how the plant interacts with the environment and how the plant defends itself against diseases. The abundance of microorganisms that are common in plant tissues is termed “plant microbiome.” ARS scientists have collaborated with scientists at West Virginia State University on a study to analyze the plant microbiome of watermelon fruits. Using advanced genomic technologies, known as meta-genomic analysis, the scientists identified a variety of microorganisms in watermelon fruits. The meta-genomic analysis also identified several types of microorganisms that might be beneficial for the human digestive system. The results in this study are useful for the scientific community concerning knowledge about beneficial microorganisms in fruits and vegetables that defend the plant against diseases. Also, the information in this study is useful for researchers and consumers who are interested in identifying microorganisms that exist in fruits and vegetables and are beneficial for human health.

Technical Abstract: The plant microbiome is a key determinant of plant health and productivity, and alteration of the plant microbiome can increase the quality of agricultural products. Little is known about the microbial population in fruit development of plants. In this study, we aimed to understand the function of microbes during fruit development and ripening of watermelon. We used 16 Svedberg units (S) metagenomics and RNAseq metatranscriptomics for analysis of red and yellow/white fruit-flesh cultivars of watermelon. Metagenomics data showed that as compared with other bacterial groups, proteobacteria were abundant in "Sweet Dakota Rose" (SDRose) and PI2 27202, whereas cyanobacteria were most abundant in the "Congo" and PI4559074. Although Bacillus are predominant in other cultivated crops, they were not widely present in the watermelon fruits. Overall, we found low bacterial diversity in watermelon fruits. This diversity could be due to the preference of microorganisms for specialized metabolic activities such as watermelon fruit flesh. A heatmap of metatranscriptomics showed Proteobacteria as the most dominant phylum in all cultivars. Among the six cultivars, SDRose exhibited lower bacterial diversity. eggNOG predicted the gene functions of microbes and associated them with lipid, amino acid metabolism and transport of molecules activities. Actinobacteria, known for biosynthesis of secondary metabolites including carbohydrates and polysaccharides, were at high levels in the JBush cultivar. However, each cultivar showed preferential abundance of different phyla. Pathway classification indicated that during the final stages of watermelon fruit development, galactose metabolism, with stachyose sequentially converted into sucrose, is critical. This study identified the presence and activity of glycoside hydrolases, carbohydrate esterases, carbohydrate binding molecules, and glycosyl transferases. The final stages of fruit development exhibited increased activity of stachyose and raffinose, determining sink strength for high sugar accumulation, and carbohydrates for fruit softening by Basidiomycota. These results underline the links between the plant-associated microbiome and the final stages of fruit development in watermelon.