Indigenous opportunistic bacteria inhabit mammalian gut-associated lymphoid tissues and share a mucosal antibody-mediated symbiosis

Abstract

The indigenous bacteria create natural cohabitation niches together with mucosal Abs in the gastrointestinal (GI) tract. Here we report that opportunistic bacteria, largely Alcaligenes species, specifically inhabit host Peyer's patches (PPs) and isolated lymphoid follicles, with the associated preferential induction of antigen-specific mucosal IgA Abs in the GI tract. Alcaligenes were identified as the dominant bacteria on the interior of PPs from naïve, specific-pathogen-free but not from germ-free mice. Oral transfer of intratissue uncultured Alcaligenes into germ-free mice resulted in the presence of Alcaligenes inside the PPs of recipients. This result was further supported by the induction of antigen-specific Ab-producing cells in the mucosal (e.g., PPs) but not systemic compartment (e.g., spleen). The preferential presence of Alcaligenes inside PPs and the associated induction of intestinal secretory IgA Abs were also observed in both monkeys and humans. Localized mucosal Ab-mediated symbiotic immune responses were supported by Alcaligenes-stimulated CD11c + dendritic cells (DCs) producing the Ab-enhancing cytokines TGF-β, B-cell-activating factor belonging to the TNF family, and IL-6 in PPs. These CD11c + DCs did not migrate beyond the draining mesenteric lymph nodes. In the absence of antigen-specific mucosal Abs, the presence of Alcaligenes in PPs was greatly diminished. Thus, indigenous opportunistic bacteria uniquely inhabit PPs, leading to PP-DCsinitiated, local antigen-specific Ab production; this may involve the creation of an optimal symbiotic environment on the interior of the PPs.Alcaligenes | intratissue habitation | Peyer's patch

Gut microbiota are linked to increased susceptibility to hepatic steatosis in low-aerobic-capacity rats fed an acute high-fat diet

“…Here, LCR rats had an increased relative abundance of the family Alicaligenaceae and genus Sutterella, which may be related to the progression of NAFLD. Patients with cirrhosis and hepatic encephalitis have low fecal concentrations of Alicaligenaceae, which has been positively associated with cognitive decline in these patients (2,40). Alicaligenaceae are known to degrade urea to ammonia, which could cause cognitive impairment; however, the involvement of this family in NAFLD is not fully understood (2,20,40).…”

“…Patients with cirrhosis and hepatic encephalitis have low fecal concentrations of Alicaligenaceae, which has been positively associated with cognitive decline in these patients (2,40). Alicaligenaceae are known to degrade urea to ammonia, which could cause cognitive impairment; however, the involvement of this family in NAFLD is not fully understood (2,20,40). Overall, we posit that increases in Proteobacteria in HCR rats are caused by an increase in endogenous nitrogen and sulfurcontaining substrates (i.e., mucins and sloughed epithelial cells) reaching the cecum.…”

The Role of Secretory Immunoglobulin A in the Natural Sensing of Commensal Bacteria by Mouse Peyer's Patch Dendritic Cells

“…A particular feature of the gastrointestinal (GI) 2 tract is the presence of a very diverse and dense microbiota comprising as many as 10 14 bacterial cells, outnumbering the amount of cells composing the human body by a factor of up to 10 (1). In addition to peacefully co-existing with the host, an equilibrium referred to as commensalism, bacteria residing in the gut exhibit numerous protective and metabolic features essential to the filter function of the epithelial barrier lining mucosal surfaces (2).…”

“…The absence of a virulence program and the differential perception of microbial-associated molecular patterns by epithelial cells may explain such a dichotomy in the host response (6). On the other hand, in IgA-deficient mice, systemic antibody (Ab) responses against commensal species are increased (7,8), changes in epithelial cell protective responses occur (9), and survival of specific bacteria is promoted (10), a collection of features all arguing for a relevant function of SIgA in the sensing mechanisms of the mucosal environment.…”

Development of a PCR-Based Method for Monitoring the Status of Alcaligenes Species in the Agricultural Environment

“…It is also unknown why Alcaligenes exclusively inhabit PPs. A study by Obata et al 2010 determined that Alcaligenes sp. can change their morphology from rod-to coccoidform.…”