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Influence of Pig Gut Microbiota on Mycoplasma Hyopneumoniae Susceptibility

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Influence of Pig Gut Microbiota on Mycoplasma Hyopneumoniae Susceptibility Surendran Nair et al. Vet Res (2019) 50:86 https://doi.org/10.1186/s13567-019-0701-8 RESEARCH ARTICLE Open Access Infuence of pig gut microbiota on Mycoplasma hyopneumoniae susceptibility Meera Surendran Nair1, Tyson Eucker2, Brian Martinson2, Axel Neubauer2, Joseph Victoria2, Bryon Nicholson2 and Maria Pieters1* Abstract This study investigated the infuence of gut microbiome composition in modulating susceptibility to Mycoplasma hyopneumoniae in pigs. Thirty-two conventional M. hyopneumoniae free piglets were randomly selected from six dif- ferent litters at 3 weeks of age and were experimentally inoculated with M. hyopneumoniae at 8 weeks of age. Lung lesion scores (LS) were recorded 4 weeks post-inoculation (12 weeks of age) from piglet lungs at necropsy. Fecal bac- terial community composition of piglets at 3, 8 and 12 weeks of age were targeted by amplifying the V3–V4 region of the 16S rRNA gene. The LS ranged from 0.3 to 43% with an evident clustering of the scores observed in piglets within litters. There were signifcant diferences in species richness and alpha diversity in fecal microbiomes among piglets within litters at diferent time points (p < 0.05). The dissimilarity matrices indicated that at 3 weeks of age, the fecal microbiota of piglets was more dissimilar compared to those from 8 to 12 weeks of age. Specifc groups of bacteria in the gut that might predict the decreased severity of M. hyopneumoniae associated lesions were identifed. The micro- bial shift at 3 weeks of age was observed to be driven by the increase in abundance of the indicator family, Rumino- coccaceae in piglets with low LS (p < 0.05). The taxa, Ruminococcus_2 having the highest richness scores, correlated signifcantly between litters showing stronger associations with the lowest LS (r 0.49, p 0.005). These fndings suggest that early life gut microbiota can be a potential determinant for M. hyopneumoniae=− = susceptibility in pigs. Introduction establishment of secondary respiratory infections by Mycoplasma hyopneumoniae is the causative agent of decreasing the ciliary motility in the respiratory tract [1, enzootic pneumonia and is considered one of the most 4]. Terefore, M. hyopneumoniae associated illness nega- important bacterial etiologies associated with chronic tively afects proftability and increases production costs, respiratory illnesses in swine production. Studies on with high morbidity in swine herds. transmission dynamics of M. hyopneumoniae indicate Controlling mycoplasma-induced pneumonia in the the continuous persistence of the bacterium within an feld is a major goal in the swine industry [1, 5]. How- infected herd via both sow-to-piglet and horizontal ever, strategies for disease control are not perfect. Farm transmission [1]. In endemically infected herds, mature management, vaccination, medication, and eradication pigs serve as pathogen reservoirs. However, grow-to-fn- are frequent tools to combat the detrimental efect of M. ish pigs often develop clinical signs [2] at a high preva- hyopneumoniae infections [6, 7]. lence, which can reach 38–100% in most production Experimental swine models have been historically systems [3]. Mycoplasma hyopneumoniae infections are used to study the pathogenesis, diagnostics, and treat- mostly characterized by non-productive chronic cough ment strategies allied with M. hyopneumoniae infection lasting weeks to months, and pave an easy path for the [8, 9]. A plethora of studies over multiple decades have described successful attempts at inducing mycoplasmal pneumonia at experimental level [9, 10]. Te associated *Correspondence: [email protected] 1 Department of Veterinary Population Medicine, University of Minnesota, lung lesions are frequently characterized by purple to St. Paul, MN, USA grey areas of pulmonary consolidation, mainly observed Full list of author information is available at the end of the article in the apical and middle lobes, as well as in the accessory © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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. Surendran Nair et al. Vet Res (2019) 50:86 Page 2 of 13 and anterior parts of the diaphragmatic lobes [10]. How- communities in the piglet gut at diferent time points, ever, variations in pneumonic lesions remain a challenge and subsequent susceptibility to develop severe myco- [9]. Several confounding variables, including possible plasma pneumonic lesions was analyzed using the 16S maternal and paternal genetic efects have been sug- rRNA fecal microbiome profling of M. hyopneumoniae gested, which could infuence the degree of mycoplasmal infected pigs. pneumonia [9, 11, 12]. A recursive partitioning analysis on determinants for experimental enzootic pneumonia Materials and methods reproduction identifed study duration, M. hyopneumo- Ethics statement niae strain, age at inoculation, co-infection with other Piglets in this study were sampled following protocols pathogens, and animal source as the most important fac- approved by Boehringer-Ingelheim Institutional Animal tors linked to the observed lung lesion score variability Care and Use Committee and handled according to the [9]. Conversely, it was observed that even after control- nursery farm standard procedures. ling for many of the aforementioned covariates, the vari- ability in lung lesions exists. Experimental design and animals Recent research indicates that changes in gut micro- Tis study consisted of repeated sampling and evaluation bial composition and function can induce alterations of 32 piglets randomly selected from six diferent litters, in respiratory mucosal immune responses and can lead over a period of 12 weeks after birth. Piglets were nega- to disease development in lungs. Several studies in this tive for M. hyopneumoniae and PRRS virus based on clin- direction have identifed the role of gut microbiota in ical history and lack of seroconversion to both pathogens, swine respiratory infections, particularly in porcine as measured by ELISA. reproductive and respiratory syndrome (PRRS), porcine Piglets born to six diferent dams at a commercial sow circovirus type 2 (PCV2), and M. hyopneumoniae [13– farm, irrespective of parity, were weaned at 3 weeks of 15]. However, mechanisms by which the gut microbiota age, transported to a research facility and were allocated could afect the pathophysiology of lungs are still in their randomly to one of six rooms. All piglets were adminis- infancy. tered ceftiofur (5 mg/kg, IM) at weaning prior to sample Early-life gut microbiota diversity and composition collection, as a part of routine farm practices. All piglets have been identifed as promising predictive biomarkers were fed a commercial diet ad libitum. A subset of thirty for health and disease in animals and humans [16–19]. piglets were housed in fve rooms (6 piglets per room) For many years, signifcant eforts have focused on the and were intra-tracheally inoculated with M. hyopneu- 5 function and composition of gut microbiota and their moniae strain 232 [22] at a dose of 1 × 10 CCU/mL at relationship with enteric diseases. To a greater extent, 8 weeks of age. Two piglets remained as uninoculated this is due to the close proximity and integral relation- controls throughout the study, and were housed sepa- ship of pathogenic and nonpathogenic microbiota in the rately in an experimental room. All piglets in this study digestive tract. Nevertheless, the feld of systemic infec- were monitored for morbidity and mortality, and clini- tious diseases is undergoing a paradigm shift as the sig- cal disease was evaluated and recorded prior to, during, nifcant role of the intestinal microbiome in response and after M. hyopneumoniae inoculation. Fecal swabs to infections outside of the gastrointestinal tract is get- were collected from all piglets at 3, 8 and 12 weeks of age, ting unveiled. For instance, in a pediatric cystic fbrosis corresponding to weaning, pre-challenge, and 4 weeks study, the patterns of acquisition of “normal microbiome” post-challenge. All samples were stored at −80 °C until and the specifc assemblages of bacteria in the gut were processing. shown to be associated with exacerbation of respiratory Piglets were humanely euthanized and necrop- illnesses in infants [18, 20]. Te fndings contributed to sied 4 weeks post-challenge, and lungs were removed, “gut-lung axis” concept, portraying the immunologic and assessed for a total percentage of M. hyopneu- cross-talk between the gut and lung mucosa [21]. Tere- moniae-suggestive lesions as described in European fore, it has been proposed that distinct composition and Pharmacopoeia [10, 23]. Total lung lesion score (LS) function of gut fora in early life can infuence host sus- was calculated for each pig using the following for- ceptibility to respiratory pathogens. mula = 100% × [(Right Apical Lobe × 11%) + (Right Based on this background information, we conducted Cardiac Lobe × 10%) + (Right Diaphragmatic an exploratory study to answer whether the gut micro- Lobe × 34%) + (Left Apical Lobe × 5%) + (Left Cardiac biome
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