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. 2022 Jun 6:13:887635.
doi: 10.3389/fpls.2022.887635. eCollection 2022.

Characterization and Comparison of Convergence Among Cephalotus follicularis Pitcher Plant-Associated Communities With Those of Nepenthes and Sarracenia Found Worldwide

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Characterization and Comparison of Convergence Among Cephalotus follicularis Pitcher Plant-Associated Communities With Those of Nepenthes and Sarracenia Found Worldwide

Leonora S Bittleston et al. Front Plant Sci. .

Abstract

The Albany pitcher plant, Cephalotus follicularis, has evolved cup-shaped leaves and a carnivorous habit completely independently from other lineages of pitcher plants. It is the only species in the family Cephalotaceae and is restricted to a small region of Western Australia. Here, we used metabarcoding to characterize the bacterial and eukaryotic communities living in C. follicularis pitchers at two different sites. Bacterial and eukaryotic communities were correlated in both richness and composition; however, the factors associated with richness were not the same across bacteria and eukaryotes, with bacterial richness differing with fluid color, and eukaryotic richness differing with the concentration of DNA extracted from the fluid, a measure roughly related to biomass. For turnover in composition, the variation in both bacterial and eukaryotic communities primarily differed with fluid acidity, fluid color, and sampling site. We compared C. follicularis-associated community diversity with that of Australian Nepenthes mirabilis, as well as a global comparison of Southeast Asian Nepenthes and North American Sarracenia. Our results showed similarity in richness with communities from other pitcher plants, and specific bacterial taxa shared among all three independent lineages of pitcher plants. Overall, we saw convergence in richness and particular clades colonizing pitcher plants around the world, suggesting that these highly specialized habitats select for certain numbers and types of inhabitants.

Keywords: bacteria; carnivorous plant; convergent evolution; eukaryote; microbe; microbiome.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Characterizing Cephalotus follicularis-associated communities. (A) Image of C. follicularis pitcher in its natural habitat (Photo credit: L.S. Bittleston). (B) Relative abundances of the most common bacterial (top) and eukaryotic (bottom) taxa across our samples. The first 20 were from site Two Peoples Bay (TPB) and the second set from Gull Rock Road (GRR). Some bacterial samples did not sequence well (Cf07, 21, 35, and 36); those columns are left blank. (C) Richness, measured as effective number of species [the exponential of Shannon diversity of the amplicon sequence variants (ASVs)] by site for bacteria (left) and eukaryotes (right). (D) Bacterial and eukaryotic richness (effective numbers of species) are correlated.
Figure 2
Figure 2
Differences in Cephalotus follicularis microbial community composition. (A–D) Beta diversity nonmetric multidimensional scaling (NMDS) plots using unweighted UniFrac distances for bacterial and eukaryotic community composition by collecting site and fluid pH. Points in plots (A) and (B) are colored by site and connected at the mean for each site, while points in plots (C) and (D) are colored by pH and overlaid with a smooth surface representing pH. (E,F) Taxonomic heat trees for bacteria and eukaryotes showing taxa significantly enriched in pitcher fluids of different colors when compared with clear fluid. Taxa shown are enriched by a log2 ratio median proportion of 3.
Figure 3
Figure 3
Global comparison of pitcher plant-associated communities. (A,B) Richness measured as effective number of species for Cephalotus follicularis bacteria (A) and eukaryotes (B) in comparison with Australian Nepenthes mirabilis, other Nepenthes, Sarracenia, and environmental communities. Different letters above the violin plots represent significant differences as measured by a pairwise Wilcoxon test, with Benjamini and Hochberg adjustment for multiple comparisons. (C,D) Phylogenetic trees of bacteria (C) and eukaryotes (D), comparing organisms from environmental samples (brown, outer ring) with those found in at least 10% of our Cephalotus follicularis (green, innermost ring), Nepenthes (red, second innermost ring) and Sarracenia (blue, second outermost ring) samples. Names of selected shared clades are listed.

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