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.
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Acknowledgements
We greatly appreciated the help of Josie Hoh and Chad Durkin at Hiʻipaka LLC. Kirsten Cannoles and Sean Swift for their assistance in the laboratory, Niranjan Gunasekara for his help setting up air samplers and during fieldwork, and Cédric Arisdakessian and Mahdi Belcaid for developing the bioinformatic pipeline used. We also appreciate the efforts of three anonymous reviewers whose insights and suggestions greatly improved this manuscript. We also acknowledge the generous support of Illumina Corporation, Michele Langner, and the ASGPB for sequencing.
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This work was supported by a grant from the W.M. Keck Foundation to ASA.
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ASA planned and designed research; all authors conducted fieldwork, analyzed data, and contributed to the paper content; VNSS prepared next-generation sequencing libraries and constructed air samplers; CBW and JB curated codes; ASA, JB, and CBW interpreted the results; and JB, CBW, MSC, RLR, and ASA wrote the paper.
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Bernard, J., Wall, C.B., Costantini, M.S. et al. Plant part and a steep environmental gradient predict plant microbial composition in a tropical watershed. ISME J 15, 999–1009 (2021). https://doi.org/10.1038/s41396-020-00826-5
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DOI: https://doi.org/10.1038/s41396-020-00826-5
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