Abstract

Plant roots in soil host a repertoire of bacteria and fungi, whose ecological interactions could improve their functions and plant performance. However, the potential microbial interactions and underlying mechanisms remain largely unknown across the soil-mangrove root interface. We herein analyzed microbial intra- and inter-domain network topologies, keystone taxa, and interaction-related genes across four compartments (non-rhizosphere, rhizosphere, episphere, and endosphere) from a soil-mangrove root continuum, using amplicon and metagenome sequencing technologies. We found that both intra- and inter-domain networks displayed notable differences in the structure and topology across four compartments. Compared to three peripheral compartments, the endosphere was a distinctive compartment harboring more dense co-occurrences with a higher average connectivity in bacterial-fungal network (2.986) than in bacterial (2.628) or fungal network (2.419), which could be related to three bacterial keystone taxa (Vibrio, Anaerolineae, and Desulfarculaceae) detected in the endosphere as they are known to intensify inter-domain associations with fungi and stimulate biofilm formation. In support of this finding, we also found that the genes involved in cell-cell communications by quorum sensing (rhlI, lasI, pqsH, and lasR) and aerobic cobamide biosynthesis (cobG, cobF, and cobA) were highly enriched in the endosphere, whereas anaerobic cobamide biosynthesis (encoded by cbiT and cbiE) was dominant in three peripheral compartments. Our results provide genetic evidence for the intensified bacterial-fungal associations of root endophytes, highlighting the critical role of the soil-root interface in structuring the microbial inter-domain associations.

Highlights

  • IntroductionThe roots of soil-grown plants host diverse microbial communities, and microbe-microbe interactions (e.g., inhibition, facilitation, and competition) are highly prevalent and have emerged as an important feature of plant root ecosystems (Gomes et al, 2011; Duran et al, 2018)

  • The roots of soil-grown plants host diverse microbial communities, and microbe-microbe interactions are highly prevalent and have emerged as an important feature of plant root ecosystems (Gomes et al, 2011; Duran et al, 2018)

  • To explore putative microbe-microbe interactions across the soil-mangrove root interface, we analyzed microbial intradomain and inter-domain co-occurrences based on sequencing datasets of bacterial and fungal communities (Figure 1A and Supplementary Table 3), which were represented as single bacterial and fungal network, and bacterial-fungal association (BFA) networks

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Summary

Introduction

The roots of soil-grown plants host diverse microbial communities, and microbe-microbe interactions (e.g., inhibition, facilitation, and competition) are highly prevalent and have emerged as an important feature of plant root ecosystems (Gomes et al, 2011; Duran et al, 2018). Inter-domain microbial interactions were enriched with negative correlations between bacteria and filamentous eukaryotes in Arabidopsis thaliana roots, where bacterial communities were essential for plant survival and protection against filamentous eukaryotes (Zhang et al, 2019) These studies contribute to the growing body of evidence that the plant growth and health are closely connected to microbial interactions from soil-root system (Duran et al, 2018), which carry out key functions like synergistic effects on plant growth, maintenance of host-microbiota balance, and protection against environmental pathogens (Duran et al, 2018). The intra- and inter-domain interactions of microbial communities, and their dynamics across the soil-root interface are poorly understood

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