A core phyllosphere microbiome exists across distant populations of a tree species indigenous to New Zealand

Abstract

The phyllosphere microbiome is increasingly recognised as an influential component of plant physiology, yet it remains unclear whether stable host-microbe associations generally exist in the phyllosphere. Leptospermum scoparium (mānuka) is a tea tree indigenous to New Zealand, and honey derived from mānuka is widely known to possess unique antimicrobial properties. However, the host physiological traits associated with these antimicrobial properties vary widely, and the specific cause of such variation has eluded scientists despite decades of research. Notably, the mānuka phyllosphere microbiome remains uncharacterised, and its potential role in mediating host physiology has not been considered. Working within the prevailing core microbiome conceptual framework, we hypothesise that the phyllosphere microbiome of mānuka exhibits specific host association patterns congruent with those of a microbial community under host selective pressure (null hypothesis: the mānuka phyllosphere microbiome is recruited stochastically from the surrounding environment). To examine our hypothesis, we characterised the phyllosphere and associated soil microbiomes of five distinct and geographically distant mānuka populations across the North Island of New Zealand. We identified a habitat-specific and relatively abundant core microbiome in the mānuka phyllosphere, which was persistent across all samples. In contrast, non-core phyllosphere microorganisms exhibited significant variation across individual host trees and populations that was strongly driven by environmental and spatial factors. Our results demonstrate the existence of a dominant and ubiquitous core microbiome in the phyllosphere of mānuka, supporting our hypothesis that phyllosphere microorganisms of mānuka exhibit specific host association and potentially mediate physiological traits of this nationally and culturally treasured indigenous plant. In addition, our results illustrate biogeographical patterns in mānuka phyllosphere microbiomes and offer insight into factors contributing to phyllosphere microbiome assembly.