Networking in the Plant Microbiome

Abstract

Almost all higher organisms, including plants, insects, and mammals, are colonized by complex microbial communities and harbor a microbiome. Emerging studies with plants reveal that these microbiomes are structured and form complex, interconnected microbial networks. Within these networks, different taxa have different roles, and keystone species have been identified that could be crucial for plant health and ecosystem functioning. A new paper in this issue of PLOS Biology by Agler et al. highlights the presence of microbial hubs in these networks that may act as mediators between the plant and its microbiome. A next major frontier is now to link microbiome composition to function. In order to do this, we present a number of hypothetical examples of how microbiome diversity and function potentially influence host performance.

Fig 1. Microbial networks vary in complexity and organization.

(A) A compartmentalized microbial network consisting of two hubs of microbial taxa that frequently interact and/or respond similarly to environmental cues. (B) A microbial network with two hubs but without modularity, as compartmentalization does not necessarily have to be observed in networks with hubs. (C) A strongly connected microbial network without hubs, where all taxa show similar degrees of interactions.

Fig 2. Co-occurrence network of microbial taxa detected in organically and conventionally managed soils by a high-throughput DNA sequencing approach of ribosomal markers (data modified after Hartmann et al., 2015 [14]).

Nodes represent over 3,000 bacterial and fungal taxa, whereas edges represent significant positive correlations between pairs of taxa. Node size corresponds to the number of connections, and taxa with many correlations are located in the densely connected areas of the network. Green nodes are microbial taxa that are significantly more abundant in organically managed plots, while red nodes are significantly more abundant in conventionally managed plots. Taxa that showed highest connectivity in the two systems, and which could be assigned at genus level, are indicated as tables in the left (organic) and right (conventional) corner of the plot (see S1 Text for further details).

Fig 3. Hypothetical relationships between microbiome diversity and plant growth response.

(A) The redundancy hypothesis predicts that plant performance increases with increasing microbiome diversity, but that saturation occurs in that further increases in diversity do not enhance performance, as additional microbial species are redundant. (B) There is no relationship between microbiome diversity and plant performance, and the plant response depends on factors such as plant species identity, the specific microbiome composition, and the biotic and abiotic environment. (C) There are alternative stable states and performance optima and minima depending on changes within the microbiome composition. For instance, the establishment of keystone species facilitates establishment of other microbes, leading to an alternative stable state. This, in turn, can alter plant performance. (D) The establishment (1) or loss (2) of a keystone species (numbered 1 or 2) has a big impact on plant responses, be it positive (as in this graph) or negative, when the presence of a pathogen reduces plant performance (modified after Naeem et al. 2002 [20]).