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. 2022 Feb 16;4(1):13.
doi: 10.1186/s42523-022-00164-1.

Bacterial communities in carnivorous pitcher plants colonize and persist in inquiline mosquitoes

Aldo A Arellano  1   2 , Kerri L Coon  3
Affiliations

Bacterial communities in carnivorous pitcher plants colonize and persist in inquiline mosquitoes

Aldo A Arellano et al. Anim Microbiome. .

Abstract

Background: The leaves of carnivorous pitcher plants harbor diverse communities of inquiline species, including bacteria and larvae of the pitcher plant mosquito (Wyeomyia smithii), which aid the plant by processing captured prey. Despite the growing appreciation for this microecosystem as a tractable model in which to study food web dynamics and the moniker of W. smithii as a 'keystone predator', very little is known about microbiota acquisition and assembly in W. smithii mosquitoes or the impacts of W. smithii-microbiota interactions on mosquito and/or plant fitness.

Results: In this study, we used high throughput sequencing of bacterial 16S rRNA gene amplicons to characterize and compare microbiota diversity in field- and laboratory-derived W. smithii larvae. We then conducted controlled experiments in the laboratory to better understand the factors shaping microbiota acquisition and persistence across the W. smithii life cycle. Methods were also developed to produce axenic (microbiota-free) W. smithii larvae that can be selectively recolonized with one or more known bacterial species in order to study microbiota function. Our results support a dominant role for the pitcher environment in shaping microbiota diversity in W. smithii larvae, while also indicating that pitcher-associated microbiota can persist in and be dispersed by adult W. smithii mosquitoes. We also demonstrate the successful generation of axenic W. smithii larvae and report variable fitness outcomes in gnotobiotic larvae monocolonized by individual bacterial isolates derived from naturally occurring pitchers in the field.

Conclusions: This study provides the first information on microbiota acquisition and assembly in W. smithii mosquitoes. This study also provides the first evidence for successful microbiota manipulation in this species. Altogether, our results highlight the value of such methods for studying host-microbiota interactions and lay the foundation for future studies to understand how W. smithii-microbiota interactions shape the structure and stability of this important model ecosystem.

Keywords: Development; Life history; Microbiota diversity; Mosquito; Wyeomyia smithii.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Relative abundance of bacterial orders in water and W. smithii larvae from naturally occurring pitchers in the field and the laboratory. Each bar presents the proportion of sequencing reads assigned to a given order. Only categories > 2% are presented
Fig. 2
Fig. 2
Ordination analyses using phylogenetic aware (PhILR, left) and unaware (clr, right) beta diversity indices. Legends in the bottom left of each plot designate sample type by the following symbol shapes/colors: red circles (field-derived larvae), green triangles (field-derived water), blue squares (lab-derived larvae), and purple crosses (lab-derived water). Ellipses designate 95% confidence intervals. Permutational multivariate analysis of variance (PERMANOVA) and permutational analysis of multivariate dispersions (PERMDISP) were used to test for group effects and heterogeneity of dispersion, respectively (see Tables 1, 2)
Fig. 3
Fig. 3
Relative abundance of bacterial orders across W. smithii life history in the laboratory. Each bar presents the proportion of sequencing reads assigned to a given order. Only categories > 2% are presented
Fig. 4
Fig. 4
Ordination analyses using phylogenetic aware (PhILR, left) and unaware (clr, right) beta diversity indices. Legends in the bottom left of each plot designate sample type by the following symbol shapes/colors: red squares (eggs), green triangles (water), yellow circles (larvae), unfilled purple stars (newly emerged adult males), filled purple stars (newly emerged adult females), unfilled blue diamonds (mature adult males), and filled blue diamonds (mature adult females). Ellipses designate 95% confidence intervals. Permutational multivariate analysis of variance (PERMANOVA) and permutational analysis of multivariate dispersions (PERMDISP) were used to test for group effects and heterogeneity of dispersion, respectively (see Tables 3, 4)
Fig. 5
Fig. 5
a Proportion of axenic first instars surviving to the pupal stage when fed: sterilized diet only (Axenic) or sterilized diet plus different bacterial isolates. Gnotobiotic larvae recolonized with the mixed community of bacteria present under conventional rearing conditions (i.e., their ‘Native microbiota’) served as the positive control. A minimum of 98 larvae were assayed per treatment across two independent assays. An asterisk (*) indicates a significant difference for a given treatment relative to the positive control (Barnard’s test; p < 0.01). b Development time of the same larvae from egg hatching to pupation. Box-and-whisker plots show high, low, and median values, with lower and upper edges of each box denoting first and third quartiles, respectively. An asterisk (*) indicates a significant difference for a given treatment relative to the positive control (Mann–Whitney U test; p < 0.01). The number above each bar represents the number of larvae that pupated and for which development time to pupation was recorded
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