Phytobiomes are compositionally nested from the ground up

Amend, Anthony S.; Cobian, Gerald M.; Láruson, Áki J.; Remple, Kristina; Tucker, Sarah J.; Poff, Kirsten E; Antaky, Carmen; Boraks, André; Jones, Casey A; Kuehu, Donna Lee; Lensing, Becca R; Pejhanmehr, Mersedeh; Richardson, Daniel T; Riley, Paul P

doi:10.7287/peerj.preprints.27393v1

Cited by 8 publications

(18 citation statements)

References 28 publications

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“…This pattern is replicated at all locations throughout our environmental gradient, and is consistent with previous studies on other plant species [19,28,61]. Although the causes of these vertically stratified patterns are undetermined, soils may inoculate plants with generalist microbes during germination, followed by additional non-random factors (e.g., desiccation, dispersal limitation) that subset the original microbial community over time and distance from the ground [19,61]. Intriguingly, rhizosphere communities, not soil, are basal in the nestedness hierarchy, congruent with previous studies [19,27].…”

Section: Effect Of Microhabitat On Microbial Distributionsupporting

confidence: 92%

“…Similar to previous studies [19,28,61], we show that microhabitat type significantly influences microbial community composition. This factor is twice as strong for bacteria as fungi (Table 1).…”

Section: Effect Of Microhabitat On Microbial Distributionsupporting

confidence: 90%

“…Although the causes of these vertically stratified patterns are undetermined, soils may inoculate plants with generalist microbes during germination, followed by additional non-random factors (e.g., desiccation, dispersal limitation) that subset the original microbial community over time and distance from the ground [19,61]. Intriguingly, rhizosphere communities, not soil, are basal in the nestedness hierarchy, congruent with previous studies [19,27]. This might reflect this microhabitat's unique mix of diverse soil-and plant-associated microbial communities in a resource rich and heterogeneous environment.…”

Section: Effect Of Microhabitat On Microbial Distributionmentioning

confidence: 99%

“…Plant-associated microbial communities can change across elevation gradients [10][11][12][13][14] or in response to soil properties (e.g., organic carbon, soil pH, nitrogen content [15] and land-use history [16]). Even in the absence of obvious environmental clines, geographic distance coupled with presumed dispersal limitation can alter microbiome composition [17][18][19]. Host identity [20] and genotype [8,21,22] can also covary with environmental factors, which can influence microbial composition as well [23].…”

Section: Introductionmentioning

confidence: 99%

“…The assembly processes governing within-plant microbial assembly is not merely a recapitulation of dispersal-or environmentally-mediated dissimilarity at a smaller scale. While large environmental clines can result in compositional turnover (i.e., replacement of species between communities) [27], microbiomes within an individual plant tend to be compositionally nested such that apical parts (e.g., leaves, flowers) house a subset of the microbial species associated with subterranean plant parts, which themselves are most species rich [19]. This nestedness pattern indicates that, although compositionally distinct, microbiomes of different Both plant part and environment shape phytobiomes Bernard et al -4 plant tissues within a plant are neither entirely independent of each other nor of the larger environmental species pool.…”

Section: Introductionmentioning

confidence: 99%

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Multiscale interactions between plant part and a steep environmental gradient determine plant microbial composition in a tropical watershed

Bernard

Wall

Costantini

et al. 2020

Preprint

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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. Interactions between these scales, however, are seldom considered. Here we analyze epiphytic microbes from nine Hibiscus tiliaceus trees across a steep 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. While the composition of microbial communities is driven primarily by microhabitat, this variable predicted more than twice the compositional variance for bacteria compared to fungi. Fungal community compositional dissimilarity increased more rapidly along the gradient than did bacteria. Additionally, the spatial dynamics of fungal communities 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 identify potential differences underlying the mechanisms shaping communities of fungi and bacteria associated with plants, and indicate an interaction between assembly mechanisms working simultaneously on different spatial scales.

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Section: Effect Of Microhabitat On Microbial Distributionsupporting

confidence: 92%

Section: Effect Of Microhabitat On Microbial Distributionsupporting

confidence: 90%

Section: Effect Of Microhabitat On Microbial Distributionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Multiscale interactions between plant part and a steep environmental gradient determine plant microbial composition in a tropical watershed

Bernard

Wall

Costantini

et al. 2020

Preprint

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Natural bacterial assemblages inArabidopsis thalianatissues become more distinguishable and diverse during host development

Beilsmith

Perisin

Bergelson

2020

Preprint

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To study the spatial and temporal dynamics of bacterial colonization under field conditions, we planted and sampled Arabidopsis thaliana during two years at two Michigan sites and surveyed colonists with 16S rRNA gene amplicon sequence variants (ASVs). Mosaic and dynamic bacterial assemblages revealed the plant as a patchwork of tissue habitats that differentiated with age. ASV prevalence patterns varied not only between roots and the phyllosphere but among phyllosphere tissues. Increasing assemblage diversity indicated that variants dispersed more widely over time, decreasing the importance of stochastic variation in early colonization relative to tissue differences. As tissues underwent developmental transitions, the root and phyllosphere assemblages became more distinct. This pattern was driven by common variants rather than those restricted to a particular tissue or transiently present at one developmental stage. Patterns also depended critically on fine phylogenetic resolution: when ASVs were grouped at coarse taxonomic levels, their associations with host tissue and age disappeared. Thus, the observed spatial and temporal variation in colonization depended upon bacterial traits that were less conserved than the family-level metabolic functions recently reported to govern ex situ plant microbiome assembly. Some colonists were consistently more successful at entering specific tissues, as evidenced by their repeatable spatial prevalence distributions across sites and years. However, these variants did not overtake plant assemblages, which instead became more even over time. Together, these results suggested that the increasing effect of tissue type was related to colonization bottlenecks for specific ASVs rather than to their ability to dominate other colonists once established. ImportanceThe efficiency with which bacteria colonize plants is an important parameter in the study of microbial community assembly and bacterial pathogenesis. We sampled roots and each emerging shoot tissue throughout an annual plant's life cycle in order to better understand where, when, and how the host influenced the bacterial portion of its microbiome in field conditions. Host plant filtering produced distinct microbiomes in roots and shoots as well as in different above-ground tissues. Mature tissue samples provided better insight into the host's role in shaping assembly since microbiome composition became more tightly linked to tissue differences, particularly between leaves and roots, as development progressed. These tissue differences disappeared at taxonomic levels higher than genus. Thus, this host effect might depend on recently acquired bacterial traits related to successful colonization of the leaf niche rather than on more deeply conserved metabolic traits.

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IMPACT OF PHYLLOSPHERE METHYLOBACTERIUM ON HOST RICE LANDRACES

Sanjenbam

Shivaprasad

Agashe

2022

Preprint

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The genus Methylobacterium includes widespread plant–associated bacteria that dominate the plant phyllosphere (occupying leaf surfaces), consume plant–secreted methanol, and can produce plant growth–promoting metabolites. However, despite the potential to increase agricultural productivity, their impact on host fitness in the natural environment is relatively poorly understood. Here, we conducted field experiments with three traditionally cultivated rice landraces from north eastern India. We inoculated seedlings with native vs. non–native phyllosphere Methylobacterium strains, finding significant impacts on plant growth and grain yield. However, these effects were variable: whereas some Methylobacterium isolates were beneficial for their host, others had no impact or were no more beneficial than the bacterial growth medium. Host plant benefits were not consistently associated with Methylobacterium colonization, altered phyllosphere microbiome composition, changes in early expression of plant stress response pathways, or bacterial auxin production. We provide the first clear demonstration of the benefits of phyllosphere Methylobacterium for rice yield under field conditions, and highlight the need for further analysis to understand the mechanisms underlying these benefits. Given that the host landrace–Methylobacterium relationship is not generalizable, future agricultural applications will require careful testing to identify coevolved host–bacterium pairs that may enhance the productivity of high-value rice varieties.

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Phytobiomes are compositionally nested from the ground up

Cited by 8 publications

References 28 publications

Multiscale interactions between plant part and a steep environmental gradient determine plant microbial composition in a tropical watershed

Multiscale interactions between plant part and a steep environmental gradient determine plant microbial composition in a tropical watershed

Natural bacterial assemblages inArabidopsis thalianatissues become more distinguishable and diverse during host development

IMPACT OF PHYLLOSPHERE METHYLOBACTERIUM ON HOST RICE LANDRACES

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