Periodontal disease is associated with increased gut colonization of pathogenic Haemophilus parainfluenzae in patients with Crohn’s disease

Sohn, Jiho; Li, Lü; Zhang, Lixia; Genco, Robert J.; Falkner, Karen L.; Tettelin, Hervé; Rowsam, Aryn M.; Smiraglia, Dominic J.; Novák, Jan; Diaz, Patricia I.; Sun, Yijun; Kirkwood, Keith L.

doi:10.1016/j.celrep.2023.112120

Cited by 20 publications

(14 citation statements)

References 61 publications

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“…Haemophilus parainfluenzae , a known respiratory pathobiont, is also a gut pathobiont, as it plays a pro-inflammatory role in Crohn’s Disease 91 , 92 . A higher abundance of Haemophilus parainfluenzae has been positively correlated with obesity and cardiometabolic disease by some 93 , but negatively associated with similar entities by others 94 , 95 .…”

Section: Discussionmentioning

confidence: 99%

Differences in gut microbiota between Dutch and South-Asian Surinamese: potential implications for type 2 diabetes mellitus

Nayman,

Schwartz,

Polmann

et al. 2024

Sci Rep

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Gut microbiota, or the collection of diverse microorganisms in a specific ecological niche, are known to significantly impact human health. Decreased gut microbiota production of short-chain fatty acids (SCFAs) has been implicated in type 2 diabetes mellitus (T2DM) disease progression. Most microbiome studies focus on ethnic majorities. This study aims to understand how the microbiome differs between an ethnic majority (the Dutch) and minority (the South-Asian Surinamese (SAS)) group with a lower and higher prevalence of T2DM, respectively. Microbiome data from the Healthy Life in an Urban Setting (HELIUS) cohort were used. Two age- and gender-matched groups were compared: the Dutch (n = 41) and SAS (n = 43). Microbial community compositions were generated via DADA2. Metrics of microbial diversity and similarity between groups were computed. Biomarker analyses were performed to determine discriminating taxa. Bacterial co-occurrence networks were constructed to examine ecological patterns. A tight microbiota cluster was observed in the Dutch women, which overlapped with some of the SAS microbiota. The Dutch gut contained a more interconnected microbial ecology, whereas the SAS network was dispersed, i.e., contained fewer inter-taxonomic correlational relationships. Bacteroides caccae, Butyricicoccus, Alistipes putredinis, Coprococcus comes, Odoribacter splanchnicus, and Lachnospira were enriched in the Dutch gut. Haemophilus, Bifidobacterium, and Anaerostipes hadrus discriminated the SAS gut. All but Lachnospira and certain strains of Haemophilus are known to produce SCFAs. The Dutch gut microbiome was distinguished from the SAS by diverse, differentially abundant SCFA-producing taxa with significant cooperation. The dynamic ecology observed in the Dutch was not detected in the SAS. Among several potential gut microbial biomarkers, Haemophilus parainfluenzae likely best characterizes the ethnic minority group, which is more predisposed to T2DM. The higher prevalence of T2DM in the SAS may be associated with the gut dysbiosis observed.

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Section: Discussionmentioning

confidence: 99%

Differences in gut microbiota between Dutch and South-Asian Surinamese: potential implications for type 2 diabetes mellitus

Nayman,

Schwartz,

Polmann

et al. 2024

Sci Rep

View full text Add to dashboard Cite

show abstract

“…Haemophilus parainfluenzae , a known respiratory pathobiont, is also a gut pathobiont, as it plays a pro-inflammatory role in Crohn’s Disease [89,90]. A higher abundance of Haemophilus parainfluenzae has been significantly positively correlated with obesity and cardiometabolic disease by some [91], but negatively associated with similar entities by others [92,93].…”

Section: Distinct Scfa-producing Gut Microbial Milieus Between Ethnic...mentioning

confidence: 99%

Disrupted Ecology andH. parainfluenzaeDistinguish the Gut Microbiota of an Ethnic Minority Predisposed to Type 2 Diabetes Mellitus

Nayman,

Schwartz,

Polmann

et al. 2023

Preprint

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PurposeDecreased gut microbiota production of short-chain fatty acids (SCFAs) has been implicated in type 2 diabetes mellitus (T2DM) disease progression. Most microbiome studies focus on ethnic majorities. This study aims to understand microbiome differences between an ethnic majority (the Dutch) and minority (the South-Asian Surinamese (SAS)) group with a lower and higher prevalence of T2DM, respectively.MethodsMicrobiome data from the Healthy Life in an Urban Setting (HELIUS) cohort were used. The 16S rRNA V4 region was sequenced. Two age– and gender-matched groups were compared: the Dutch (n = 41) and SAS (n = 43). Microbial compositions were generated via DADA2. Alpha and beta-diversity and Principal Coordinate Analysis (PCoA) were computed. DESeq2 differential bacterial abundance and LEfSe biomarker analyses were performed to determine discriminating features. Co-occurrence networks were constructed to examine gut ecology.ResultsA tight cluster of bacterial abundances was observed in the Dutch women, which overlapped with some of the SAS microbiomes. The Dutch gut contained a more interconnected microbial ecology, whereas the SAS network was dispersed.Bacteroides caccae, Butyricicoccus, Alistipes putredinis, Coprococcus comes,Odoribacter splanchnicus,andLachnospiracharacterized the Dutch gut.Haemophilus,Bifidobacterium,andAnaerostipes hadruscharacterized the SAS gut. All butLachnospiraand certain strains ofHaemophilusare known SCFA producers.ConclusionThe Dutch gut microbiome was distinguished from the SAS by diverse, differentially abundant SCFA-producing taxa with significant cooperation. The dynamic ecology observed in the Dutch was lost in the SAS. The higher prevalence of T2DM in the SAS may be associated with the dysbiosis observed.

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“… 17 Of note, consistent with animal studies, periodontitis is associated with increased gut colonization by an oral pathobiont Haemophilus parainfluenzae in patients with Crohn’s disease (CD). 18 Thus, oral pathobionts, expanded during oral inflammation, contribute to the pathogenesis of GI diseases through ectopic colonization in the gut mucosa.…”

Section: Introductionmentioning

confidence: 99%

Oral pathobiont Klebsiella chaperon usher pili provide site-specific adaptation for the inflamed gut mucosa

Guo,

Kitamoto,

Caballero-Flores

et al. 2024

Gut Microbes

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The ectopic gut colonization by orally derived pathobionts has been implicated in the pathogenesis of various gastrointestinal diseases, including inflammatory bowel disease (IBD). For example, gut colonization by orally derived Klebsiella spp. has been linked to IBD in mice and humans. However, the mechanisms whereby oral pathobionts colonize extra-oral niches, such as the gut mucosa, remain largely unknown. Here, we performed a high-density transposon (Tn) screening to identify genes required for the adaptation of an oral Klebsiella strain to different mucosal sites – the oral and gut mucosae – at the steady state and during inflammation. We find that K. aerogenes , an oral pathobiont associated with both oral and gut inflammation in mice, harbors a newly identified genomic locus named “locus of colonization in the inflamed gut (LIG)” that encodes genes related to iron acquisition (Sit and Chu) and host adhesion (chaperon usher pili [CUP] system). The LIG locus is highly conserved among K. aerogenes strains, and these genes are also present in several other Klebsiella species. The Tn screening revealed that the LIG locus is required for the adaptation of K. aerogenes in its ectopic niche. In particular, we determined K. aerogenes employs a CUP system (CUP1) present in the LIG locus for colonization in the inflamed gut, but not in the oral mucosa. Thus, oral pathobionts likely exploit distinct adaptation mechanisms in their ectopically colonized intestinal niche compared to their native niche.

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Periodontal disease is associated with increased gut colonization of pathogenic Haemophilus parainfluenzae in patients with Crohn’s disease

Cited by 20 publications

References 61 publications

Differences in gut microbiota between Dutch and South-Asian Surinamese: potential implications for type 2 diabetes mellitus

Differences in gut microbiota between Dutch and South-Asian Surinamese: potential implications for type 2 diabetes mellitus

Disrupted Ecology andH. parainfluenzaeDistinguish the Gut Microbiota of an Ethnic Minority Predisposed to Type 2 Diabetes Mellitus

Oral pathobiont Klebsiella chaperon usher pili provide site-specific adaptation for the inflamed gut mucosa

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