Abstract

Macropod progressive periodontal disease (MPPD) is a necrotizing, polymicrobial, inflammatory disease commonly diagnosed in captive macropods. MPPD is characterized by gingivitis associated with dental plaque formation, which progresses to periodontitis and then to osteomyelitis of the mandible or maxilla. However, the underlying microbial causes of this disease remain poorly understood. In this study, we collected 27 oral plaque samples and associated clinical records from 22 captive Macropodidae and Potoroidae individuals that were undergoing clinical examination at Adelaide and Monarto Zoos in South Australia (15 healthy, 7 gingivitis and 5 periodontitis-osteomyelitis samples). The V3-V4 region of the 16S ribosomal RNA gene was sequenced using an Illumina Miseq to explore links between MPPD and oral bacteria in these animals. Compositional differences were detected between the microbiota of periodontitis-osteomyelitis cases compared to healthy samples (p-value with Bonferroni correction < 0.01), as well as gingivitis cases compared to healthy samples (p-value with Bonferroni correction < 0.05) using Permutational Multivariate Analysis of Variance (PERMANOVA). An overabundance of Porphyromonas, Fusobacterium, and Bacteroides taxa was also identified in animals with MPPD compared to healthy individuals using linear discriminant analysis effect size (LEfSe; p = < 0.05). An increased abundance of Desulfomicrobium also was detected in MPPD samples (LEfSe; p < 0.05), which could potentially reflect differences in disease progression. This is the first microbiota analysis of MPPD in captive macropods, and these results support a polymicrobial pathogenesis of MPPD, suggesting that the microbial interactions underpinning MPPD may be more complex than previously documented.

Highlights

  • Macropods, which include kangaroos and wallabies, are herbivorous marsupials in the superfamily Macropodoidea within the order Diprotodontia

  • The relative abundances of bacteria at the phylum, genus, and species taxonomic levels were explored in 27 animals belonging to healthy, gingivitis and periodontitis-osteomyelitis categories

  • We have profiled the shift in oral microbiota of captive macropods at different stages of Macropod progressive periodontal disease (MPPD), as well as characterised the healthy gingival microbiome

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Summary

Introduction

Macropods, which include kangaroos and wallabies, are herbivorous marsupials in the superfamily Macropodoidea within the order Diprotodontia. Incisors are Centre for Antimicrobial Resistance Ecology, School of Animal and Veterinary Sciences, The University of Adelaide, Roseworthy, SA 5371, Australia. Macropod progressive periodontal disease (MPPD), commonly termed ‘lumpy jaw’, is a necrotising polymicrobial dental disease characterised by the proliferation of anaerobic bacteria. Reported risk factors for MPPD include stressors (e.g. cold, wet weather and overcrowding), molar progression, food impaction and plaque accumulation, faecal contamination of feed areas, age, and inappropriate ­diet[7,8,9]. Gingivitis, a reversible form of PD, presents as inflammation of gingivae resulting from the host’s innate and adaptive immune response to bacterial toxins, including enzymes, structural components and leukotoxins. Periodontitis, an irreversible form of PD, progresses to loss of integrity of the gingival epithelium and inflammation of the periodontal ligament, absorption of alveolar bone, tooth mobility and eventual tooth ­loss[4,5,6]

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