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. 2022 Jul 27;17(7):e0270913.
doi: 10.1371/journal.pone.0270913. eCollection 2022.

Illuminating protist diversity in pitcher plants and bromeliad tanks

Robin S Sleith  1 , Laura A Katz  1   2
Affiliations

Illuminating protist diversity in pitcher plants and bromeliad tanks

Robin S Sleith et al. PLoS One. .

Abstract

Many species of plants have evolved structures called phytotelmata that store water and trap detritus and prey. These structures house diverse communities of organisms, the inquiline microbiome, that aids breakdown of litter and prey. The invertebrate and bacterial food webs in these systems are well characterized, but less is known about microbial eukaryotic community dynamics. In this study we focus on microbes in the SAR clade (Stramenopila, Alveolata, Rhizaria) inhabiting phytotelmata. Using small subunit rDNA amplicon sequencing from repeated temporal and geographic samples of wild and cultivated plants across the Northeast U.S.A., we demonstrate that communities are variable within and between host plant type. Across habitats, communities from tropical bromeliads grown in a single room of a greenhouse were nearly as heterogeneous as wild pitcher plants spread across hundreds of kilometers. At the scale of pitcher plants in a single bog, analyses of samples from three time points suggest that seasonality is a major driver of protist community structure, with variable spring communities transitioning to more homogeneous communities that resemble the surrounding habitat. Our results indicate that protist communities in phytotelmata are variable, likely due to stochastic founder events and colonization/competition dynamics, leading to tremendous heterogeneity in inquiline microeukaryotic communities.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. The 135 focal OTUs from across plant hosts and geography illustrate generalist OTUs (i.e. not restricted by plant host or geography) and specialist OTUs (i.e. restricted by plant host or geography).
Branches are colored by major clades, Rhizaria (Rhi, orange) Stramenopila (Str, green) and Alveolata (Alv, blue, with Ci indicating ciliates). The number of reads is indicated in the inner ring, followed by host plant specificity (>90% of reads from a given host), followed by geographic specificity (>90% of reads from a given location).
Fig 2
Fig 2
A. OTU richness (rarefaction plots, error bars are standard deviations) and Shannon diversity (inset beanplots) is highest in samples from the background community (light blue), followed by samples collected from Sarracenia (purple), bromeliads (brown), and Nepenthes (green). B. Principal Coordinate Analysis based on weighted UNIFRAC demonstrates differentiation of communities by host plant, with tremendous heterogeneity among communities in field-collections from Sarracenia (purple dots) and among greenhouse bromeliads (brown triangles; all from the same room in the Lyman Conservatory). Details on site and OTUs can be found in S1 and S2 Files.
Fig 3
Fig 3. Network analysis demonstrates that most OTUs in a rosette of 3 pitchers are shared with the bog water below the rosette.
Connection of OTUs (circles) shared (lines) between pitchers (purple squares) and bog water (blue square) for the rosette of pitchers at Hawley Bog closest to the forest edge, sampled on May 6th ("Day 1"). Taxonomy of OTUs is colored as Rhizaria (orange) Stramenopila (green) and Alveolata (blue).
Fig 4
Fig 4
A. Principal Coordinate Analysis based on weighted UNIFRAC of communities from repeated sampling along a transect (26m from Forest Edge to Pool Edge) at Hawley Bog (May 6th ("Day 1", green); May 29th ("Day 24", purple); June 27th ("Day 53", yellow)) shows Sarracenia SAR communities in late June (Day 53, yellow filled symbols mostly appear on right side of PC1) clustering near the background community (all open symbols). B. Principal Coordinate Analysis based on weighted UNIFRAC of OTUs (same ordination space as 4A), showing that the OTUs that differentiate and correspond to the late June samples (the yellow, Day 53 samples on right side of PC1 in 4A) are primarily Alveolate OTUs (denoted in blue). Details on site and OTUs can be found in S1 and S2 Files.
Fig 5
Fig 5
The changes in relative abundance of the OTUs from each sampling month separated by sampling type (background bog water (left) vs pitchers (right); OTUs from discussion labeled) shows that the relative abundance of OTUs assigned to Rhizaria declines sharply over the growing season in pitchers, though much less drastically in the background samples. At the same time, the relative abundance of alveolates increases. Stacked barplots represent relative abundance (denoted by bar segment size and shading).
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Grants and funding

This work is supported by an NSF grant DEB-1541511 to Laura A. Katz. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.