Driving factors of epiphytic bacterial communities: A review

Abstract

Bacteria establish complex, compositionally consistent communities on healthy leaves. Ecological processes such as dispersal, diversification, ecological drift, and selection as well as leaf surface physicochemistry and topology impact community assembly. Since the leaf surface is an oligotrophic environment, species interactions such as competition and cooperation may be major contributors to shape community structure. Furthermore, the plant immune system impacts on microbial community composition, as plant cells respond to bacterial molecules and shape their responses according to the mixture of molecules present. Such tunability of the plant immune network likely enables the plant host to differentiate between pathogenic and non-pathogenic colonisers, avoiding costly immune responses to non-pathogenic colonisers. Plant immune responses are either systemically distributed or locally confined, which in turn affects the colonisation pattern of the associated microbiota. However, how each of these factors impacts the bacterial community is unclear. To better understand this impact, bacterial communities need to be studied at a micrometre resolution, which is the scale that is relevant to the members of the community. Here, current insights into the driving factors influencing the assembly of leaf surface-colonising bacterial communities are discussed, with a special focus on plant host immunity as an emerging factor contributing to bacterial leaf colonisation.

Keywords: Assembly processes; Microbial communities; Phyllosphere; Plant immunity; Single cell; Spatially explicit.

Graphical abstract

Fig. 1

(A) Representation of an Arabidopsis thaliana leaf and its main features. (B) Cross-section and (C) top-view representations of the leaf surface, including different epidermal cell types that make up the leaf's surface relief.

Fig. 2

Relevance of spatial patterns in bacterial community structure on the leaf surface. (A) Considering a plant host with a defined microbial composition and relative abundance of species 1 and 2, factors driving community structure, i.e., dispersal, diversification, ecological drift, and selection, can lead to different aggregation patterns of these species while maintaining the same bacterial diversity and abundance. (B) Bacterial community of species 1 and 2 with a strong spatial co-aggregation pattern influenced by, for example, cooperation, resource partitioning, stochastic processes, and/or priority effects (niche modification). (C) Bacterial community of species 1 and 2 with a strong spatial segregation pattern influenced by resource overlap-driven exploitation competition, antibiosis (interference competition), stochastic processes, and/or priority effects (niche preemption). (D) Bacterial community of species 1 and 2 showing a random distribution, which might indicate benign interactions between the species.

Fig. 3

Plant responses to bacterial colonisation. Leaf-colonising bacteria elicit local and systemic responses. As shown on the left-hand side, a cell type-specific response to prevent bacteria from entering the apoplast is stomatal closure. As shown on the right-hand side, plants perceive bacteria via receptors localised in the plasma membrane (A, B, C, D), which recognise microbe-associated molecular patterns (depicted by hexagons, ovals and stars around the bacterium). Downstream signaling of these receptors is integrated in a highly interconnected immune signaling network. Integration of varying receptor inputs leads to specific immune outputs (α, β, γ).