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. 2015 Jul 14:6:526.
doi: 10.3389/fmicb.2015.00526. eCollection 2015.

Metatranscriptome analysis reveals host-microbiome interactions in traps of carnivorous Genlisea species

Hieu X Cao  1 , Thomas Schmutzer  1 , Uwe Scholz  1 , Ales Pecinka  2 , Ingo Schubert  3 , Giang T H Vu  1
Affiliations

Metatranscriptome analysis reveals host-microbiome interactions in traps of carnivorous Genlisea species

Hieu X Cao et al. Front Microbiol. .

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.

Keywords: Genlisea; RNA-sequencing; algae commensalism; lobster pot trapping; metatranscriptomics; plant carnivory; plant-microbe interaction; whole-genome gene transcription analysis.

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Figures

Figure 1
Figure 1
Morphology and (micro)biome composition in Genlisea traps. (A) G. hispidula has only filiform rhizophylls, while G. nigrocaulis displays a trap dimorphism with thick, short-stalked surface traps and filiform, long-stalked deep-soil traps. (B) Relative abundance and occurrence of microbe genera of five categories: bacteria, SAR protists (Stramenopiles, Alveolata, and Rhizaria), metazoans and other eukaryotic microbes. Occurrence reflects the number of times a specific genus is found across the 8 different Genlisea metatranscriptome libraries. (C,D) Number of genera in Genlisea traps according to species (C) or season (D). The active-(micro)biome of Genlisea traps containing preferentially entrapped genera is defined as (i) ≥0.1% relative abundance among each of the five categories; (ii) occurred at least in two trap samples regardless of species or seasonal sampling time; and (iii) trap enrichment with ≥2-fold-change of abundance between traps and leaves. Asterisk indicates significant difference (p < 0.05, paired Student's t-Test). HIS, G. hispidula; NIG, G. nigrocaulis; SS, summer season; WS, winter season.
Figure 2
Figure 2
The active-(micro)biome of Genlisea traps contains 92 preferentially entrapped genera. Relative abundance, frequency of appearance in samples and relative fold change of abundance in trap vs. leaf are shown. Definition of preferentially trapped genera can be found in the legend of Figure 1. ∞ indicates trap exclusive presence.
Figure 3
Figure 3
Phenotype profiling of bacterial communities between Genlisea trap samples vs. Genlisea leaves or soil samples. Phenotype information of habitat (A), mobility (B), oxygen requirement (C), energy resources (D), and metabolisms (E,F) was extracted from the METAGENassist database.
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