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The Oral and Conjunctival Microbiotas in Cats with and Without Feline

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The Oral and Conjunctival Microbiotas in Cats with and Without Feline The oral and conjunctival microbiotas in cats with and without feline immunodeficiency virus infection Scott J Weese, Jamieson Nichols, Mohammad Jalali, Annette Litster To cite this version: Scott J Weese, Jamieson Nichols, Mohammad Jalali, Annette Litster. The oral and conjunctival microbiotas in cats with and without feline immunodeficiency virus infection. Veterinary Research, BioMed Central, 2015, 46 (1), pp.21. 10.1186/s13567-014-0140-5. hal-01290670 HAL Id: hal-01290670 https://hal.archives-ouvertes.fr/hal-01290670 Submitted on 18 Mar 2016 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Weese et al. Veterinary Research (2015) 46:21 DOI 10.1186/s13567-014-0140-5 VETERINARY RESEARCH RESEARCH Open Access The oral and conjunctival microbiotas in cats with and without feline immunodeficiency virus infection Scott J Weese1*, Jamieson Nichols2, Mohammad Jalali1 and Annette Litster2 Abstract The oral and conjunctival microbiotas likely play important roles in protection from opportunistic infections, while also being the source of potential pathogens. Yet, there has been limited investigation in cats, and the impact of comorbidities such as feline immunodeficiency virus (FIV) infection has not been reported. Oral and conjunctival swabs were collected from cats with FIV infection and FIV-uninfected controls, and subjected to 16S rRNA gene (V4) PCR and next generation sequencing. 9,249 OTUs were identified from conjunctival swabs, yet the most common 20 (0.22%) OTUs accounted for 76% of sequences. The two most abundant OTUs both belonged to Staphylococcus,and accounted for 37% of sequences. Cats with FIV infection had significantly lower relative abundances of Verrucomicrobia, Fibrobacteres, Spirochaetes, Bacteroidetes and Tenericutes, and a higher relative abundance of Deinococcus-Thermus. There were significant differences in both community membership (P = 0.006) and community structure (P =0.02) between FIV-infected and FIV-uninfected cats. FIV-infected cats had significantly higher relative abundances of Fusobacteria and Actinobacteria in the oral cavity, and significantly higher relative abundances of several bacterial classes including Fusobacteria (0.022 vs 0.007, P = 0.006), Actinobacteria (0.017 vs 0.003, P = 0.003), Sphingobacteria (0.00015 vs 0.00003, P = 0.0013) and Flavobacteria (0.0073 vs 0.0034, P = 0.030). The feline conjunctival and oral microbiotas are complex polymicrobial communities but dominated by a limited number of genera. There is an apparent impact of FIV infection on various components of the microbiota, and assessment of the clinical relevance of these alterations in required. Introduction alterations in the local microbiota play a role in the The body harbours vast microbial communities (microbio- pathophysiology of some of these diseases. Further, the tas) at different body sites [1]. The microbiota interacts oral microbiota in humans has been shown to have an closely with the immune system and alterations in the influence on various infectious diseases, including both immune status of the host can result in changes in the oral (e.g. gingivitis, stomatitis, periodontitis) and extra- microbiota, as has been shown with the fecal, anal and oral oral (e.g. infective endocarditis) disease, and alterations microbiotasofhumanswith human immunodeficiency of the oral microbiota have been identified in individ- virus (HIV) infection [2-5]. Feline immunodeficiency virus uals with HIV infection [2,12-14]. (FIV), another lentivirus, is disseminated in the cat Understanding of the normal ocular and oral microbio- population worldwide [6-10]. As with HIV in humans, tas, and changes that occur in response to FIV infection, is FIV infection can result in progressive immune dysfunction, important for understanding the impact of FIV infection with a corresponding increase in a variety of infectious dis- and the pathophysiology of FIV-associated opportunistic ease risks. A variety of ocular and oral manifestations of infections. The objectives of this study were to describe HIV infection can occur in humans, including both infec- the conjunctival and oral bacterial microbiotas and to tious and non-infectious causes [11], and it is possible that evaluate the impact of FIV infection. * Correspondence: [email protected] 1Department of Pathobiology, University of Guelph, Guelph, Canada Full list of author information is available at the end of the article © 2015 Weese et al.; licensee BioMed Central. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Weese et al. Veterinary Research (2015) 46:21 Page 2 of 11 Materials and methods Data analysis Study population Mothur v1.33.3 [17] was used to assemble paired end reads Thirty-three cats were enrolled from a broader 5-year and perform downstream analysis. After assembly, sequence longitudinal controlled study investigating the clinical ef- files were depleted of sequences that were not consistent fects of FIV in naturally acquired infection. FIV infection with the target amplicon size (240 bp), contained any am- status at the time of enrollment was determined by FIV biguous base calls or long runs (>8 bp) of holopolymers, or antibody detectiona and later confirmed using polymerase did not align with the correct 16S rRNA gene region. After chain reaction (PCR) for FIV RNAb or virus isolationc.Of alignment with the Silva 16S rRNA reference database [18], the enrolled cats, 19 were FIV-infected and 14 were FIV- chimeras were detected using UCHIME [19] and removed. uninfected. The cats enrolled in this study represent a Taxonomy was then assigned using the RDP taxonomy convenience sample based on the timing of examination database [20] and any non-bacterial sequences that remained and sample collection for the larger study. FIV-infected were removed. Sequences were then binned into operational cats were sourced from either a feline sanctuary (n =15) taxon units (OTUs) at a 3% dissimilarity level. or were privately owned (n = 4). FIV-uninfected cats were Wilcoxon signed rank tests were used to compare sourced from either the same feline sanctuary (n =2)or relative abundances of different phylogenetic groups. were privately owned (n = 12). FIV-infected and unin- Subsampling was performed to normalize sequence num- fected cats were housed indoors and comingled within ber for subsequent analyses [21] through random selection the sanctuary. Two of the privately owned cats, one FIV- of a number of sequences that was chosen to optimize infected and one FIV-uninfected, were allowed out- both sequence numbers and the number of samples doors. None of the privately owned FIV-uninfected cats that could be included. Good’s coverage, diversity (in- in this study were housed with FIV-infected cats. At the verse Simpson’s index), evenness (Shannon’sevenness time of examination, all cats were re-tested for FIV index) and richness (Catchall) [22] were calculated and antibodies. compared between groups using Wilcoxon signed rank Physical examination was performed at the time of sam- test. Dendrograms were developed based on the Yue pling. Oral and conjunctival swab samples were collected and Clayton measure of dissimilarity (a measure of with a sterile Dacron swab from the oral cavity or conjunc- community structure, which considers shared OTUs tival surface, respectively. Oral health and gingival score and their relative abundances) and traditional Jaccard were determined by visual inspection at the time of exam- index (a measure of community membership, which ination. The presence of gingivitis, stomatitis, gum reces- just considers the number of shared OTUs, not their sion, tooth root or furcation exposure, purulent material abundance) and UniFrac [23] and analysis of molecular at the gumline, loose teeth or masses was considered variance (AMOVA) were applied to compare microbial evidence of dental disease. The gingival score was deter- communities. Analysis of molecular variance was also mined using the following scale: 0 – normal gingiva with used to compare communities. Principal coordinate ana- sharp, non-inflamed edges; 1 – marginal gingivitis, minimal lysis (PCoA) and indicator analysis [24] were also per- inflammation at free margin, no bleeding when pressure formed. A P value of ≤ 0.05 was considered significant for applied to the gingiva; 2 – moderate gingivitis, wider of all analyses. inflammation at gingival margin, bleeding when pressure applied to gingiva; 3 – marked gingivitis, severe inflamma- tion, bleeding can be present or absent when pressure Results applied to gingiva [15]. As cats were conscious during Cats ranged in age from 5 to 12 years of age (median examinations, probing
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