Secreted pitfall-trap fluid of carnivorous Nepenthes plants is unsuitable for microbial growth

Buch, Franziska; Rott, Matthias; Rottloff, Sandy; Paetz, Christian; Hilke, Ines; Raessler, M.; Mithöfer, Axel

doi:10.1093/aob/mcs287

Cited by 72 publications

(73 citation statements)

References 31 publications

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“…Compared to Sarracenia, the pitcher fluid in Nepenthes contained higher activity of digestive enzymes with higher concentrations of antibacterial agents making more extreme conditions for adaptation of the bacteria [9,44]. Recent studies have attempted to assess the bacterial community in cultivated Nepenthes pitchers from 16S rRNA gene sequences by using the clonal library method [26,45]. However, the diversity generated by this method was limited by the depth of sequencing (i.e., number of sequences per sample).…”

Section: Discussionmentioning

confidence: 99%

Comparative Study of Bacterial Communities in Nepenthes Pitchers and Their Correlation to Species and Fluid Acidity

et al. 2016

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Pitchers are specialized digestive organs of carnivorous plants which evolved for trapping prey and represent a unique environment harboring hidden diversity of unexplored microbes forming transient hydrolytic microcosms. In this study, the diversity of bacterial communities in the pitcher fluids of seven local Nepenthes found in Thailand was assessed by tagged 16S ribosomal RNA (rRNA) gene amplicon sequencing on an Ion PGM™ platform. A total of 1,101,000 filtered sequences were obtained which were taxonomically classified into 20 phyla, 48 classes, 72 orders, 153 families, and 442 genera while the remainder (1.43 %) could not be assigned to any existing taxa. Proteobacteria represented the predominant members in closed pitchers and more diversified bacterial taxa particularly Bacteriodetes and Actinobacteria, showed increasing abundance in open pitchers containing insect bodies. Principal coordinate analysis revealed that distribution of bacterial taxa was not significantly related to the Nepenthes species but strongly correlated to the pH of the pitcher fluids (pH 1.7-6.7). Acidicella was a highly dominant bacterial genus in acidic pitcher fluids while Dyella and Mycobacterium were also common genera in most pitchers. A unique microbial community structure was found in Nepenthes ampullaria which could reflect their adaptation to digest leaf litter, in addition to insect prey. The work revealed the highly unexplored nature of bacterial microcosms in Nepenthes pitcher fluids and provides insights into their community structure in this unique ecological system.

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Section: Discussionmentioning

confidence: 99%

Comparative Study of Bacterial Communities in Nepenthes Pitchers and Their Correlation to Species and Fluid Acidity

et al. 2016

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“…Although indirect evidence for the former are available for Nepenthes [15,16], these studies are not without criticism, and do not demonstrate unequivocally the benefit derived from microbial colonization of its pitchers. By contrast, a growing number of studies in more recent years have shown that pitcher secretions are anti-microbial, an observation that seems to point in the direction of an antagonistic relationship between plant and fluid microbes [17][18][19].…”

Section: Introductionmentioning

confidence: 95%

Dipteran larvae and microbes facilitate nutrient sequestration in theNepenthes gracilispitcher plant host

et al. 2017

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The fluid-containing traps of Nepenthes carnivorous pitcher plants (Nepenthaceae) are often inhabited by organisms known as inquilines. Dipteran larvae are key components of such communities and are thought to facilitate pitcher nitrogen sequestration by converting prey protein into inorganic nitrogen, although this has never been demonstrated in Nepenthes. Pitcher fluids are also inhabited by microbes, although the relationship(s) between these and the plant is still unclear. In this study, we examined the hypothesis of digestive mutualism between N. gracilis pitchers and both dipteran larvae and fluid microbes. Using dipteran larvae, prey and fluid volumes mimicking in situ pitcher conditions, we conducted in vitro experiments and measured changes in available fluid nitrogen in response to dipteran larvae and microbe presence. We showed that the presence of dipteran larvae resulted in significantly higher and faster releases of ammonium and soluble protein into fluids in artificial pitchers, and that the presence of fluid microbes did likewise for ammonium. We showed also that niche segregation occurs between phorid and culicid larvae, with the former fragmenting prey carcasses and the latter suppressing fluid microbe levels. These results clarify the relationships between several key pitcher-dwelling organisms, and show that pitcher communities facilitate nutrient sequestration in their host.

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“…However, we hypothesized that Nepenthes and Sarracenia could have different microbial biota because of certain specific characteristics. First, the fluid in unopened Nepenthes pitchers may already contain microbes ( [8,62]; but see [6]), the origin of which is still uncertain, although they may come from the phyllosphere. In contrast, it was reported that Sarracenia pitchers are sterile before opening [22,49,50], so prey and/or debris falling into the pitchers may facilitate the initial microbial colonization after pitcher opening.…”

Section: Introductionmentioning

confidence: 99%

Bacterial diversity and composition in the fluid of pitcher plants of the genus Nepenthes

Takeuchi

Chaffron

Salcher

et al. 2015

Systematic and Applied Microbiology

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Pitchers are modified leaves used by carnivorous plants for trapping prey. Their fluids contain digestive enzymes from the plant and they harbor abundant microbes. In this study, the diversity of bacterial communities was assessed in Nepenthes pitcher fluids and the composition of the bacterial community was compared to that in other environments, including the phyllosphere of Arabidopsis, animal guts and another pitcher plant, Sarracenia. Diversity was measured by 454 pyrosequencing of 16S rRNA gene amplicons. A total of 232,823 sequences were obtained after chimera and singleton removal that clustered into 3260 distinct operational taxonomic units (OTUs) (3% dissimilarity), which were taxonomically distributed over 17 phyla, 25 classes, 45 orders, 100 families, and 195 genera. Pyrosequencing and fluorescence in situ hybridization yielded similar estimates of community composition. Most pitchers contained high proportions of unique OTUs, and only 22 OTUs (<0.6%) were shared by ≥14/16 samples, suggesting a unique bacterial assemblage in each pitcher at the OTU level. Diversity analysis at the class level revealed that the bacterial communities of both opened and unopened pitchers were most similar to that of Sarracenia and to that in the phyllosphere. Therefore, the bacterial community in pitchers may be formed by environmental filtering and/or by phyllosphere bacteria.

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Secreted pitfall-trap fluid of carnivorous Nepenthes plants is unsuitable for microbial growth

Cited by 72 publications

References 31 publications

Comparative Study of Bacterial Communities in Nepenthes Pitchers and Their Correlation to Species and Fluid Acidity

Comparative Study of Bacterial Communities in Nepenthes Pitchers and Their Correlation to Species and Fluid Acidity

Dipteran larvae and microbes facilitate nutrient sequestration in theNepenthes gracilispitcher plant host

Bacterial diversity and composition in the fluid of pitcher plants of the genus Nepenthes

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