Distinctive Structure and Assembly of Phyllosphere Microbial Communities between Wild and Cultivated Rice

Abstract

Wild rice has been demonstrated to possess enriched genetic diversity and multiple valuable traits involved in disease/pest resistance and abiotic stress tolerance, which provides a potential resource for sustainable agriculture. However, unlike the plant compartments such as rhizosphere, the structure and assembly of phyllosphere microbial communities of wild rice remain largely unexplored. Through amplicon sequencing, this study compared the phyllosphere bacterial and fungal communities of wild rice and its neighboring cultivated rice. The core phyllosphere microbial taxa of both wild and cultivated rice are dominated with Pantoea, Methylobacterium, Nigrospora, and Papiliotrema, which are potentially beneficial to rice growth and health. Compared to the cultivated rice, Methylobacterium, Sphingomonas, Phaeosphaeria, and Khuskia were significantly enriched in the wild rice phyllosphere. The potentially nitrogen-fixing Methylobacterium is the dominated wild-enriched microbe; Sphingomonas is the hub taxon of wild rice networks. In addition, the microbiota of wild rice was more governed by deterministic assembly with a more complicated and stable community network than the cultivated rice. Our study provides a list of the beneficial microbes in the wild rice phyllosphere and reveals the microbial divergence between wild rice and cultivated rice in the original habitats, which highlights the potential selective role of wild rice in recruiting specific microbiomes for enhancing crop performance and promoting sustainable food production. IMPORTANCE Plant microbiota are being considered a lever to increase the sustainability of food production under a changing climate. In particular, the microbiomes associated with ancestors of modern cultivars have the potential to support their domesticated cultivars. However, few efforts have been devoted to studying the biodiversity and functions of microbial communities in the native habitats of ancestors of modern crop species. This study provides a list of the beneficial microbes in the wild rice phyllosphere and explores the microbial interaction patterns and the functional profiles of wild rice. This information could be useful for the future utilization of the plant microbiome to enhance crop performance and sustainability, especially in the framework of sustainable agroecosystems.

Keywords: Methylobacterium; community assembly; cooccurrence network; core microbiome; microbial community; phyllosphere; wild rice.

FIG 1

Taxonomic profiles of microbial communities in wild and cultivated rice phyllosphere from different sites. The relative abundance of bacteria (A) and fungi (B) at genus level present in the rice phyllosphere. The Shannon index of bacterial (C) and fungal (D) communities in each rice type. The PCoA analysis of bacterial (E) and fungal (F) communities based on Bray-Curtis distances grouped by rice types and sites. (QHW, wild rice in Qionghai; WCW, wild rice in Wenchang; WNW, wild rice in Wanning; QHC, cultivated rice in Qionghai; WCC, cultivated rice in Wenchang; WNC, cultivated rice in Wanning.)

FIG 2

The shared core microbial taxa between wild and cultivated rice from different sites. Thirty-seven core bacterial taxa (A) and 29 core fungal taxa (B) were detected across all rice phyllosphere samples, as depicted by the Venn diagram. Neighbor-joining (NJ) phylogenetic trees and corresponding bar diagrams illustrating the 37 core bacterial (C) and 29 core fungal ASVs (D) (with 95% similarity as the cutoff value) and their relative abundances in all samples.

FIG 3

Specific differences of wild versus cultivated-enriched taxa. (A) Diverse bacterial and fungal taxa were enriched or depleted in the phyllosphere of wild rice relative to cultivated rice. Each point represents one amplicon sequence variant (ASV) and was labeled as the closest matching species based on comparison to the NCBI sequence database using BLAST. The relative abundance of main enriched phyllosphere BASVs (B) and FASVs (C) of wild rice and cultivated rice, respectively.

FIG 4

Predicted functional profiles of the rice phyllosphere microbiome. (A) Functional prediction of core and enriched BASVs in wild rice and cultivated rice using FAPROTAX, respectively. Only significant differences between wild and cultivated rice were compared using FDR-corrected Wilcoxon’s test (*, P < 0.05; **, P < 0.01). (B) Stamp analysis showed the significantly different fungal functional groups among enriched FASVs of wild rice and cultivated rice.

FIG 5

Interkingdom cooccurrence networks. (A) Networks contained both bacterial and fungal taxa showing a higher number of nodes and edges in the wild rice network than those in the cultivated rice network. Positive and negative relationships are illustrated in gray and green, respectively. Degree (B) and clustering coefficient values (C) of nodes and number of bacterial–bacterial (BB), bacterial–fungal (BF), and fungal–fungal (FF) correlations (D) in wild and cultivated rice networks. (E) Comparison of node-level topological features in panel A demonstrating the high degree and closeness centrality values for the hub taxa. Taxonomic information of the hub taxa is presented in Tables S8 and S9. (F) Degree and interaction type of the top 10 hub nodes in wild and cultivated rice networks. “Intra-kingdom correlation” refers to BB or FF, and “interkingdom correlation” refers to BF.

FIG 6

Community assembly of wild and cultivated rice phyllosphere microbial communities. Sloan neutral model prediction of wild rice bacterial (A) and fungal (B) communities and cultivated rice bacterial (C) and fungal (D) communities, indicated by R² values (fit to neutral assembly process) and m values (estimated migration rate). ASVs are represented by data points and colored according to whether the taxon fit above (red), within (black), or below (blue) the 95% confidence interval (dashed lines). (E) The relative importance of five ecological processes of wild and cultivated rice phyllosphere microbial communities. (F) Comparison of mean community-level habitat niche breadths of bacterial and fungal taxa among wild and cultivated rice phyllosphere.