Heritable Gut Microbiome Associated with Salmonella enterica Serovar Pullorum Infection in Chickens

Abstract

Pullorum disease is one of the most common diarrhea-related diseases caused by Salmonella enterica subspecies enterica serovar Gallinarum biovar Pullorum (S. Pullorum); it negatively affects the poultry industry. However, limited studies have explored the association between the gut microbiota and S. Pullorum infection in chickens. In the present study, we performed a microbiome comparison and a microbiome genome-wide association study (mGWAS) to investigate the association among the host genetics, the gut microbiota, and pullorum disease in chickens. We found that S. Pullorum infection in chickens could alter the abundance of 39 bacterial genera (P < 0.05). The altered structure and composition of the gut microbiota were also detected in the offspring. mGWAS results revealed host genetic variants to be prominently associated with gut microbial diversity and individual microbes. The pathogens Pelomonas and Brevundimonas, which had a high abundance in positive parent chickens and their offspring, were significantly associated with several genetic mutations in immunity-related genes, such as TGIF1, TTLL12, and CCR7. This finding explained why Pelomonas and Brevundimonas were heritable in S. Pullorum-infected chickens. The heritable gut microbes and identified genetic variants could provide references for the selection of resistant chickens and the elimination of pullorum disease. IMPORTANCE The present study investigated the association among the host genome, the gut microbiome, and S. Pullorum infection in chickens. The results suggested that the gut microbial structure is altered in S. Pullorum-infected chickens. The diversity and abundance of the gut microbiota remarkably differed between the offspring coming from S. Pullorum-positive and S. Pullorum-negative chickens. Heritable gut microbiota were detected in the offspring. Moreover, host genetic variants were associated with microbial diversity and individual gut microbes. The pathogens Pelomonas and Brevundimonas, which exhibited a high heritability in S. Pullorum-positive parents and their offspring, were associated with several genetic mutations in immunity-related genes.

Effects of a probiotic-fermented herbal blend on the growth performance, intestinal flora and immune function of chicks infected with Salmonella pullorum

“…After invading the digestive tract of chicks, S. pullorum preferentially targets the cloacal bursa and spleen prior to eliciting inflammation in the intestine and causing systemic infection ( Shivaprasad and Barrow, 2007 ; Ding et al., 2021 ). The immunity of young chicks is extremely immature and, therefore, not able to trigger a cellular immune response robust enough to avoid systemic infection.…”

Strength Lies in Diversity: How Community Diversity Limits Salmonella Abundance in the Chicken Intestine

“…While other studies have reported negative or positive correlations between intestinal community composition, abundance of specific genera/species and Salmonella abundance or prevalence ( Videnska et al, 2013 ; Azcarate-Peril et al, 2018 ), this has been a tenuous association as reflected in comparisons among studies ( Azcarate-Peril et al, 2018 ; Ma et al, 2020 ; Mon et al, 2020 ) and trials ( Videnska et al, 2013 ). The exclusive genera/species, identified in this study, have been associated with Salmonella exclusion in some studies ( Pourabedin et al, 2017 ; Liu et al, 2018 ; Khan and Chousalkar, 2020 ; Ding et al, 2021 ), but absent in others ( Videnska et al, 2013 ; Azcarate-Peril et al, 2018 ; Ma et al, 2020 ; Mon et al, 2020 ). The genera/species, identified in this study, that negatively correlate with Salmonella are also absent in a competitive exclusion product known to effectively reduce Salmonella colonization in poultry ( Pedroso et al, 2016 ).…”

“…These genera or species have also been associated with enteropathogen colonization or intestinal health in other studies ( Antharam et al, 2013 ; Miquel et al, 2013 ; Rossi et al, 2014 ; Stanley et al, 2014 ; Xu et al, 2014 ; Thibodeau et al, 2015 ; Knoll et al, 2016 ). Others have also noted absence or reduced abundance of F. prausnitzii and member species of the clostridial families ( Collins et al, 1994 ) Lachnospiraceae (XIV) and Ruminococcaceae (III/IV) in birds colonized with Salmonella ( Pourabedin et al, 2017 ; Liu et al, 2018 ; Khan and Chousalkar, 2020 ; Ding et al, 2021 ). Several of these species, associated with exclusive communities but absent from the Salmonella permissive community, may play an anti-inflammatory role in maintaining intestinal homeostasis and health ( Wu and Wu, 2012 ; Miquel et al, 2013 ).…”

Dynamic distribution of gut microbiota during Alzheimer's disease progression in a mice model

“…The sequencing and barcode primers were removed from the reads for the identification of the V4 sequence. The sequence reads were filtered by related settings, as in our previous study [22]. Briefly, the pair‐end sequence reads passed our quality control standards (average mass >30, sequence length >50) and was assembled according to their overlapping sequences.…”