Our study shows that intensive antibiotic treatment in sows severely affected the microbial communities inhabiting piglets’ noses. This effect was more pronounced when using a combination of crystalline ceftiofur and tulathromycin than only using crystalline ceftiofur. Both sow treatments affected the bacterial transfer from sows to piglets, which showed a nasal microbiota with reduced alpha diversity and decreased populations of commonly found swine nasal colonizers; the addition of an extra administration of ceftiofur to new-born piglets had no further effect.
The low transfer of microbiota from the sows seemed to increase the detection in the piglets’ nasal cavities of uncommon bacteria for this niche, with taxa from the orders Burkholderiales and Rhizobiales (Ralstonia, Afipia and Hyphomicrobium) among the most abundant ones. These microorganisms are not found in the nasal microbiota of pigs under standard farm conditions and are unlikely to be part of the swine nasal microbiota. These taxa are often associated with plants, as symbionts or pathogens [62, 63] and they probably came from the food or the extraction kit in the case of Ralstonia, as it has been shown in other studies [64]. The detection of environmental microbes in high relative abundance could be caused by the reduced presence of professional colonizers, creating a low-biomass environment prone to be colonized by transit microorganisms, as it has been previously observed [65]. In agreement, during the pre-processing of raw reads, we found Chloroplast and Mitochondrial 16S signals in unusual high abundances (9.5% and 4.3%, respectively) in comparison with the farm animals evaluated in this study, as well as in previous studies (0.07% and 0.03%, respectively) [5, 8].
Despite finding the stated unusual microbes, the rest of the microbiota was constituted of taxa previously found in swine respiratory microbiota [5, 7, 8, 30, 66–68], which includes aerobic taxa as well as gut-associated anaerobic taxa that are commonly found and shown to be active in the pig’s nose [69]. Nevertheless, all of them were initially detected in a very low abundance (considering also the 16S rRNA gene qPCR) and were represented by an unusual low quantity of ASVs. Altogether, these results suggest that the antibiotic treatment had a drastic effect on these microorganisms. This is in agreement with several studies assessing the effect of antibiotic treatments on the microbiota [5, 30, 33, 35, 70]. As Mou et al. (2019) have confirmed, pig nasal microbiota shifted in response to the broad-spectrum antibiotic oxytetracycline treatment, normally used to treat respiratory bacterial diseases in swine (including Mycoplasma, Pasteurella and Glaesserella). They determined that oxytetracycline administered orally had a major impact in the diversity and disturbance of the microbiota than the intramuscular route [30]. In the present study, we only assessed the intramuscular administration and observed that ceftiofur and tulathromycin administered by this route was enough to severely disturb the nasal microbiota and avoid the bacterial transfer from sow to piglet. In particular, sow antibiotic treatment reduced drastically the bacterial transfer of natural nasal microbiota members, being among the three pathobionts G. parasuis, M. hyorhinis and S. suis. Although G. parasuis was not found in any of the sows, it is known that the level of this bacterium in nasal swabs from sows is sometimes too low to be detectable [16]. The results obtained by PCR in piglets could be explained if the animals carried G. parasuis strains sensitive to tulathromycin but resistant to ceftiofur. This could be attributed to the presence of plasmids that bear resistances to β-lactams, as the ROB-1 β-lactamase reported in the pB1000 and the pJMA-1 plasmids. These plasmids were found in strains recovered from the nasal cavities from healthy animals and considered non-virulent strains [71]. In the case of S. suis, the transmission of this pathogen from sow to piglet seems to be prevented. However, we cannot discard the presence of S. suis in tonsils, since we have not analysed this niche, which is preferentially colonized by this bacterium [67]. Similarly, M. hyorhinis colonization in piglets seems to have been prevented, but it is also possible that this colonization could occur later in life [17].
In farms, the antibiotic treatments given to the sows are intended to reduce pathogen transmission to the piglets. However, our results indicate that these interventions can also have negative consequences, since the dysbiosis produced by these drugs could facilitate pathogen colonization, with the consequent higher risk of infection. In fact, we detected in piglets from treated sows some potentials pathogens such as Acinetobacter [72, 73], Clostridium [74] or Treponema [75] that were not found in the farm samples. In good health status farms, the colonization of these pathogens is probably controlled by the exclusion provided by the normal nasal microbiota. Other explanation could be the selection of resistant strains from these potential pathogens. In agreement, Acinetobacter was detected together with eighteen different antibiotics in the groundwater of areas affected by swine farming [72]. Moreover, the poorly establishment of the microbiota in the early ages of the animal live could determine the proper maturation of their immune system [76].
Although several studies have demonstrated that the use of antimicrobial drugs in sows have an important impact on the establishment of the microbiota in the firsts weeks of life of their offspring [7], and the effect of these drugs could last longer when administered to the sows compared to the administrations to their piglets [35], we have not studied this effect in a long-term period, as we only had piglet nasal swabs from one timepoint (D22-24). It would have been very interesting to elucidate the impact of the transitory effect of these antimicrobials in an extended period of time.
In conclusion, our results evidenced the importance of the maternal microbiota in the first establishment of the respiratory microbiota of piglets and control of potential pathogens. This should be taken into consideration when setting treatment plans and routines in swine industry.