Abstract

Orange-tufted sunbirds (Cinnyris osea) feed on the nectar of the tobacco tree (Nicotiana glauca) which contains toxic pyridine alkaloids characterized by high concentrations of anabasine and much lower concentrations of nicotine. We aimed at determining whether the gut microbiota of sunbirds harbors bacterial species that enable the birds to cope with these toxic alkaloids. An in vivo experiment that included 12 birds showed that inducing dysbiosis in sunbirds’ guts by the addition of sulfamethoxazole and trimethoprim, significantly reduced the birds’ ability to degrade anabasine (n = 3) compared to control birds (n = 3) with undisturbed microbiota. Sunbirds whose gut bacterial communities were altered by the antibacterial agents and who were fed with added nicotine, also showed a lower percentage of nicotine degradation (n = 3) in their excreta compared to the sunbirds with undisturbed microbiota (n = 3), though this difference was not significant. In an in vitro experiment, we studied the ability of Lactococcus lactis, Enterobacter hormaechei, Chryseobacterium gleum, Kocuria palustris, and Methylorubrum populi that were isolated from sunbirds’ excreta, to degrade anabasine and nicotine. By using gas chromatography-mass spectrometry (GC-MS) analysis, we successfully demonstrated, for the first time, the ability of these species to degrade the focal secondary metabolites. Our findings demonstrate the role of gut bacteria in detoxifying toxic secondary metabolites found in the N. glauca nectar. The degradation products may supply the birds with nitrogen which is scarce in nectar-rich diets. These findings support another role of bacteria in mediating the interactions between plants and their pollinators.

Highlights

  • Microbiota are a collection of microorganisms that inhabit a specific environment, while a microbiome is a collection of genes and genomes of members of a microbiota (Marchesi and Ravel, 2015)

  • Twelve birds were used for the in vivo experiment (Figure 1). These birds were divided into two groups; the birds in group G1 were tested for their ability to degrade anabasine, while the birds in group G2 were tested for their ability to degrade nicotine

  • After 72 h of the antibacterial agent treatment, anabasine was added to the diets of all birds in group G1 and nicotine was added to the diets of all birds in group G2 (Figure 1)

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Summary

Introduction

Microbiota are a collection of microorganisms that inhabit a specific environment, while a microbiome is a collection of genes and genomes of members of a microbiota (Marchesi and Ravel, 2015). The study of avian gut microbial diversity and function focuses mostly on commercial bird species such as turkeys and chickens (Grond et al, 2018). Preest and Beuchat (2003) isolated bacteria from Anna’s hummingbird, and Lee et al (2019) and Gunasekaran et al (2020) molecularly analyzed the microbial community of hummingbirds and sunbirds excreta, respectively. These studies suggested that nectarivorous birds lack large ceca, they possess a diverse bacterial community (278 ASVs) in their gut (Gunasekaran et al, 2020)

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