Abstract
In the carnivorous plant genus Genlisea a unique lobster pot trapping mechanism supplements nutrition in nutrient-poor habitats. A wide spectrum of microbes frequently occurs in Genlisea's leaf-derived traps without clear relevance for Genlisea carnivory. We sequenced the metatranscriptomes of subterrestrial traps vs. the aerial chlorophyll-containing leaves of G. nigrocaulis and of G. hispidula. Ribosomal RNA assignment revealed soil-borne microbial diversity in Genlisea traps, with 92 genera of 19 phyla present in more than one sample. Microbes from 16 of these phyla including proteobacteria, green algae, amoebozoa, fungi, ciliates and metazoans, contributed additionally short-lived mRNA to the metatranscriptome. Furthermore, transcripts of 438 members of hydrolases (e.g., proteases, phosphatases, lipases), mainly resembling those of metazoans, ciliates and green algae, were found. Compared to aerial leaves, Genlisea traps displayed a transcriptional up-regulation of endogenous NADH oxidases generating reactive oxygen species as well as of acid phosphatases for prey digestion. A leaf-vs.-trap transcriptome comparison reflects that carnivory provides inorganic P- and different forms of N-compounds (ammonium, nitrate, amino acid, oligopeptides) and implies the need to protect trap cells against oxidative stress. The analysis elucidates a complex food web inside the Genlisea traps, and suggests ecological relationships between this plant genus and its entrapped microbiome.
Highlights
Carnivory, including trapping and subsequent digestion of prey, has evolved several times in plants
Trap-Specific Enrichment among the Highly Diverse and Dynamic Phylotypes of Genlisea Traps Deep sequencing has been shown to be a suitable approach for large-scale comparisons of microbial communities (Caporaso et al, 2011; Yarza et al, 2014)
Overall we found in Genlisea trap samples 184 out of total 220 uniquely detected genera having at least 0.1% relative abundance of either bacteria, SAR protists (Stramenopiles, Alveolata and Rhizaria), green algae (Chlorophyta), metazoa, or other eukaryotic microbes (Figure 1B)
Summary
Carnivory, including trapping and subsequent digestion of prey, has evolved several times in plants. Carnivorous plants are distributed worldwide, their occurrence is ecologically restricted to open, wet, nutrient-poor habitats. This indicates that the nutritional benefit from carnivory supports survival of carnivorous plants in such environments. Inside the Utricularia and Genlisea traps, diverse microbial communities, mainly comprising bacteria, algae, protozoa and rotifers, could live as epiphytes or parasites or might support plant fitness in the context of prey digestion before or without becoming digested themselves (Skutch, 1928; Jobson and Morris, 2001; Richards, 2001; Sirová et al, 2003, 2009; Płachno et al, 2005; Adamec, 2007; Plachno and Wolowski, 2008; Caravieri et al, 2014). Specialized soil microbes with high biomass-degrading capacity could be selected or cultivated, for example in an herbivore microbiome of the leaf-cutter ant (Atta colombica) (Suen et al, 2010)
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