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Microbial Population Differentials between Mucosal and Submucosal Intestinal Tissues in Advanced Crohn's Disease of the Ileum.

Chiodini RJ, Dowd SE, Chamberlin WM, Galandiuk S, Davis B, Glassing A - PLoS ONE (2015)

Bottom Line: A variety of organisms of the Phylum Firmicutes were increased in the subjacent submucosa as compared to the parallel mucosal tissue including Ruminococcus spp., Oscillospira spp., Pseudobutyrivibrio spp., and Tumebacillus spp.In addition, Propionibacterium spp. and Cloacibacterium spp. were increased as well as large increases in Proteobacteria including Parasutterella spp. and Methylobacterium spp.Our data demonstrate the existence of a distinct submucosal microbiome and ecosystem that is not well reflected in the mucosa and/or downstream fecal material.

View Article: PubMed Central - PubMed

Affiliation: St. Vincent Healthcare, Sisters of Charity of Leavenworth Health System, Billings, Montana, United States of America; Department of Biological and Physical Sciences, Montana State University-Billings, Billings, Montana, United States of America.

ABSTRACT
Since Crohn's disease is a transmural disease, we hypothesized that examination of deep submucosal tissues directly involved in the inflammatory disease process may provide unique insights into bacterial populations transgressing intestinal barriers and bacterial populations more representative of the causes and agents of the disease. We performed deep 16s microbiota sequencing on isolated ilea mucosal and submucosal tissues on 20 patients with Crohn's disease and 15 non-inflammatory bowel disease controls with a depth of coverage averaging 81,500 sequences in each of the 70 DNA samples yielding an overall resolution down to 0.0001% of the bacterial population. Of the 4,802,328 total sequences generated, 98.9% or 4,749,183 sequences aligned with the Kingdom Bacteria that clustered into 8545 unique sequences with <3% divergence or operational taxonomic units enabling the identification of 401 genera and 698 tentative bacterial species. There were significant differences in all taxonomic levels between the submucosal microbiota in Crohn's disease compared to controls, including organisms of the Order Desulfovibrionales that were present within the submucosal tissues of most Crohn's disease patients but absent in the control group. A variety of organisms of the Phylum Firmicutes were increased in the subjacent submucosa as compared to the parallel mucosal tissue including Ruminococcus spp., Oscillospira spp., Pseudobutyrivibrio spp., and Tumebacillus spp. In addition, Propionibacterium spp. and Cloacibacterium spp. were increased as well as large increases in Proteobacteria including Parasutterella spp. and Methylobacterium spp. This is the first study to examine the microbial populations within submucosal tissues of patients with Crohn's disease and to compare microbial communities found deep within the submucosal tissues with those present on mucosal surfaces. Our data demonstrate the existence of a distinct submucosal microbiome and ecosystem that is not well reflected in the mucosa and/or downstream fecal material.

No MeSH data available.


Related in: MedlinePlus

Comparison of the relative abundance of bacterial Orders within the submucosa of the diseased ileum in Crohn's disease as compared to the ileal submucosa in nIBD controls.Various Orders, such as Selenomonadales and Rhizobiales, are absent or poorly represented with the mucosa of Crohn's disease tissue while other orders such as Desulfovibrionales and Coriobacteriales are absent or poorly represented in nIBD controls. Panel A: Relative abundance within submucosal tissues of each bacterial Order in each disease group. Panel B: Relative comparison and contribution of each Order to the total. Legend: Bacteria present in less than 50% of patients are excluded. All data presented are statistically significant (p = <0.05).
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pone.0134382.g007: Comparison of the relative abundance of bacterial Orders within the submucosa of the diseased ileum in Crohn's disease as compared to the ileal submucosa in nIBD controls.Various Orders, such as Selenomonadales and Rhizobiales, are absent or poorly represented with the mucosa of Crohn's disease tissue while other orders such as Desulfovibrionales and Coriobacteriales are absent or poorly represented in nIBD controls. Panel A: Relative abundance within submucosal tissues of each bacterial Order in each disease group. Panel B: Relative comparison and contribution of each Order to the total. Legend: Bacteria present in less than 50% of patients are excluded. All data presented are statistically significant (p = <0.05).

Mentions: Most notably, at the Phylum level, Tenericutes were 60-fold higher (p = 0.001) and Fusobacteria were 6-fold higher (p = 0.01) within Crohn's disease submucosal tissues as compared to nIBD controls. At the taxonomic level of Class, there were significant differences in 7 of the 34 classes detected including increases within the submucosa of Bacteroidia (4 fold increase; p = 0.009), Clostridia (3.5 fold increase; p = 0.007), Fusobacteria (5.6 fold increase; p = 0.03) as compared to nIBD controls. In addition, Coriobacteria were detected in 17 of 20 (85%) submucosal tissues from Crohn's disease but not in the submucosa of any nIBD control (p = 0.004). Conversely, Negativicutes were detected in the submucosa of 11 of 15 nIBD controls (79%) but not in the submucosa of a single Crohn's disease patient. Similar changes were noted at the Order taxonomic level with major differences between the submucosal microbiota in ileal Crohn's disease and in nIBD controls (Fig 7) including a 25-fold increase in bacteria of the Order Coriobacteriales (p = 0.001) and a 6–7 fold increase in bacteria of the order Bifidobacteriales (p = 0.03) and Fusobacteriales (p = 0.02) within the submucosa of Crohn's disease as compared to nIBD controls. As was noted at the Class level, organisms of the Order Selenomonadales and Rhizobiales were absent or near absent in the submucosal tissue of Crohn's disease as opposed to nIBD controls (p = 0.003 and p = 0.002, respectively) and, conversely, bacteria of the order Coriobacteriales and Desulfovibrionales present in nIBD controls where absent or near absent within the submucosal tissues in Crohn's disease (p = 0.001 and p = 0.02, respectively) (Fig 7).


Microbial Population Differentials between Mucosal and Submucosal Intestinal Tissues in Advanced Crohn's Disease of the Ileum.

Chiodini RJ, Dowd SE, Chamberlin WM, Galandiuk S, Davis B, Glassing A - PLoS ONE (2015)

Comparison of the relative abundance of bacterial Orders within the submucosa of the diseased ileum in Crohn's disease as compared to the ileal submucosa in nIBD controls.Various Orders, such as Selenomonadales and Rhizobiales, are absent or poorly represented with the mucosa of Crohn's disease tissue while other orders such as Desulfovibrionales and Coriobacteriales are absent or poorly represented in nIBD controls. Panel A: Relative abundance within submucosal tissues of each bacterial Order in each disease group. Panel B: Relative comparison and contribution of each Order to the total. Legend: Bacteria present in less than 50% of patients are excluded. All data presented are statistically significant (p = <0.05).
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4519195&req=5

pone.0134382.g007: Comparison of the relative abundance of bacterial Orders within the submucosa of the diseased ileum in Crohn's disease as compared to the ileal submucosa in nIBD controls.Various Orders, such as Selenomonadales and Rhizobiales, are absent or poorly represented with the mucosa of Crohn's disease tissue while other orders such as Desulfovibrionales and Coriobacteriales are absent or poorly represented in nIBD controls. Panel A: Relative abundance within submucosal tissues of each bacterial Order in each disease group. Panel B: Relative comparison and contribution of each Order to the total. Legend: Bacteria present in less than 50% of patients are excluded. All data presented are statistically significant (p = <0.05).
Mentions: Most notably, at the Phylum level, Tenericutes were 60-fold higher (p = 0.001) and Fusobacteria were 6-fold higher (p = 0.01) within Crohn's disease submucosal tissues as compared to nIBD controls. At the taxonomic level of Class, there were significant differences in 7 of the 34 classes detected including increases within the submucosa of Bacteroidia (4 fold increase; p = 0.009), Clostridia (3.5 fold increase; p = 0.007), Fusobacteria (5.6 fold increase; p = 0.03) as compared to nIBD controls. In addition, Coriobacteria were detected in 17 of 20 (85%) submucosal tissues from Crohn's disease but not in the submucosa of any nIBD control (p = 0.004). Conversely, Negativicutes were detected in the submucosa of 11 of 15 nIBD controls (79%) but not in the submucosa of a single Crohn's disease patient. Similar changes were noted at the Order taxonomic level with major differences between the submucosal microbiota in ileal Crohn's disease and in nIBD controls (Fig 7) including a 25-fold increase in bacteria of the Order Coriobacteriales (p = 0.001) and a 6–7 fold increase in bacteria of the order Bifidobacteriales (p = 0.03) and Fusobacteriales (p = 0.02) within the submucosa of Crohn's disease as compared to nIBD controls. As was noted at the Class level, organisms of the Order Selenomonadales and Rhizobiales were absent or near absent in the submucosal tissue of Crohn's disease as opposed to nIBD controls (p = 0.003 and p = 0.002, respectively) and, conversely, bacteria of the order Coriobacteriales and Desulfovibrionales present in nIBD controls where absent or near absent within the submucosal tissues in Crohn's disease (p = 0.001 and p = 0.02, respectively) (Fig 7).

Bottom Line: A variety of organisms of the Phylum Firmicutes were increased in the subjacent submucosa as compared to the parallel mucosal tissue including Ruminococcus spp., Oscillospira spp., Pseudobutyrivibrio spp., and Tumebacillus spp.In addition, Propionibacterium spp. and Cloacibacterium spp. were increased as well as large increases in Proteobacteria including Parasutterella spp. and Methylobacterium spp.Our data demonstrate the existence of a distinct submucosal microbiome and ecosystem that is not well reflected in the mucosa and/or downstream fecal material.

View Article: PubMed Central - PubMed

Affiliation: St. Vincent Healthcare, Sisters of Charity of Leavenworth Health System, Billings, Montana, United States of America; Department of Biological and Physical Sciences, Montana State University-Billings, Billings, Montana, United States of America.

ABSTRACT
Since Crohn's disease is a transmural disease, we hypothesized that examination of deep submucosal tissues directly involved in the inflammatory disease process may provide unique insights into bacterial populations transgressing intestinal barriers and bacterial populations more representative of the causes and agents of the disease. We performed deep 16s microbiota sequencing on isolated ilea mucosal and submucosal tissues on 20 patients with Crohn's disease and 15 non-inflammatory bowel disease controls with a depth of coverage averaging 81,500 sequences in each of the 70 DNA samples yielding an overall resolution down to 0.0001% of the bacterial population. Of the 4,802,328 total sequences generated, 98.9% or 4,749,183 sequences aligned with the Kingdom Bacteria that clustered into 8545 unique sequences with <3% divergence or operational taxonomic units enabling the identification of 401 genera and 698 tentative bacterial species. There were significant differences in all taxonomic levels between the submucosal microbiota in Crohn's disease compared to controls, including organisms of the Order Desulfovibrionales that were present within the submucosal tissues of most Crohn's disease patients but absent in the control group. A variety of organisms of the Phylum Firmicutes were increased in the subjacent submucosa as compared to the parallel mucosal tissue including Ruminococcus spp., Oscillospira spp., Pseudobutyrivibrio spp., and Tumebacillus spp. In addition, Propionibacterium spp. and Cloacibacterium spp. were increased as well as large increases in Proteobacteria including Parasutterella spp. and Methylobacterium spp. This is the first study to examine the microbial populations within submucosal tissues of patients with Crohn's disease and to compare microbial communities found deep within the submucosal tissues with those present on mucosal surfaces. Our data demonstrate the existence of a distinct submucosal microbiome and ecosystem that is not well reflected in the mucosa and/or downstream fecal material.

No MeSH data available.


Related in: MedlinePlus