Plant part and a steep environmental gradient predict plant microbial composition in a tropical watershed

Abstract

Plant microbiomes are shaped by forces working at different spatial scales. Environmental factors determine a pool of potential symbionts while host physiochemical factors influence how those microbes associate with distinct plant tissues. These scales are seldom considered simultaneously, despite their potential to interact. Here, we analyze epiphytic microbes from nine Hibiscus tiliaceus trees across a steep, but short, environmental gradient within a single Hawaiian watershed. At each location, we sampled eight microhabitats: leaves, petioles, axils, stems, roots, and litter from the plant, as well as surrounding air and soil. The composition of bacterial communities is better explained by microhabitat, while location better predicted compositional variance for fungi. Fungal community compositional dissimilarity increased more rapidly along the gradient than did bacterial composition. Additionally, the rates of fungal community compositional dissimilarity along the gradient differed among plant parts, and these differences influenced the distribution patterns and range size of individual taxa. Within plants, microbes were compositionally nested such that aboveground communities contained a subset of the diversity found belowground. Our findings indicate that both environmental context and microhabitat contribute to microbial compositional variance in our study, but that these contributions are influenced by the domain of microbe and the specific microhabitat in question, suggesting a complicated and potentially interacting dynamic.

Bacterial Succession and Community Dynamics of the Emerging Leaf Phyllosphere in Spring

“…As we sampled only four trees per city, we may be overestimating the amount of core taxa defined per city and compartment. Nevertheless, our findings are in accordance with previous studies that included multiple plant compartments, as they also observed many shared bacterial taxa despite the consistent observations of different phyllosphere compartments harboring very distinct community compositions ( 27 – 30 ).…”

Fungi in soil and understory have coupled distribution patterns

“…An important distinction in our study is that we sampled from the organic soil layer rather than leaf litter. Evidence from bacterial ( Bai et al, 2015 ; Zarraonaindia et al, 2015 ; Wagner et al, 2016 ) and fungal systems ( Amend et al, 2019 ; Bernard et al, 2021 ) have shown that soil may act as a reservoir of microbes that migrate to the phylloplane, an observation that is supported by our results ( Table 1 ).…”

“…Range size and niche breadth are positively correlated among plants and animals ( Slatyer, Hirst & Sexton, 2013 ; Bernard et al, 2021 ). Here we show that for fungi, niche breadth may or may not correlate with range size, and that this equivocal result depends on how range size is calculated ( Figs.…”

“…Brown’s resource-use hypothesis remains a central topic in ecology ( Slatyer, Hirst & Sexton, 2013 ; Sheth, Morueta-Holme & Angert, 2020 ) but it is seldom examined for microbes, especially fungi. A recent study of plant associated fungi showed that habitat breadth was a strong predictor of the range size over a 5 km gradient ( Bernard et al, 2021 ). These preliminary results suggest that fungi adhere to similar niche breadth –range size correlations that are observed in plants and animals.…”

“…If there is community membership overlap among the soil and phylloplane, is the overlap spatially autocorrelated? Range size has is often correlated with niche breadth ( Slatyer, Hirst & Sexton, 2013 ; Bernard et al, 2021 ) so we investigated the relationship between habitat specificity and range size. Range size can refer to a number of different measurements ( Brown, Stevens & Kaufman, 1996 ), so for the purpose of this study, range size is the geographic area occupied by an OTU within a transect.…”