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Title: Comparative genetics of Enterococcus faecalis intestinal tissue isolates before and after surgery in a rat model of colon anastomosis

Abstract

We have recently demonstrated that collagenolytic Enterococcus faecalis plays a key and causative role in the pathogenesis of anastomotic leak, an uncommon but potentially lethal complication characterized by disruption of the intestinal wound following segmental removal of the colon (resection) and its reconnection (anastomosis). Here we hypothesized that comparative genetic analysis of E. faecalis isolates present at the anastomotic wound site before and after surgery would shed insight into the mechanisms by which collagenolytic strains are selected for and predominate at sites of anastomotic disruption. Whole genome optical mapping of four pairs of isolates from rat colonic tissue obtained following surgical resection (herein named "pre-op" isolates) and then 6 days later from the anastomotic site (herein named "post-op" isolates) demonstrated that the isolates with higher collagenolytic activity formed a distinct cluster. In order to perform analysis at a deeper level, a single pair of E. faecalis isolates (16A pre-op and 16A post-op) was selected for whole genome sequencing and assembled using a hybrid assembly algorithm. Comparative genomics demonstrated absence of multiple gene clusters, notably a pathogenicity island in the post-op isolate. No differences were found in the fsr-gelE-sprE genes (EF1817-1822) responsible for regulation and production of collagenolytic activity. Analysis ofmore » unique genes among the 16A pre-op and post-op isolates revealed the predominance of transporter systems-related genes in the pre-op isolate and phage-related and hydrolytic enzyme-encoding genes in the post-op isolate. Despite genetic differences observed between pre-op and post-op isolates, the precise genetic determinants responsible for their differential expression of collagenolytic activity remains unknown.« less

Authors:
 [1];  [1];  [1];  [1];  [1];  [2];  [3];  [1]; ORCiD logo [1]
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  1. Univ. of Chicago, IL (United States)
  2. Argonne National Lab. (ANL), Argonne, IL (United States)
  3. Univ. of Chicago, IL (United States); Argonne National Lab. (ANL), Argonne, IL (United States)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
National Institutes of Health (NIH); USDOE
OSTI Identifier:
1668066
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 15; Journal Issue: 4; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Christley, Scott, Shogan, Benjamin, Levine, Zoe, Koo, Hyun, Guyton, Kristina, Owens, Sarah, Gilbert, Jack, Zaborina, Olga, and Alverdy, John C. Comparative genetics of Enterococcus faecalis intestinal tissue isolates before and after surgery in a rat model of colon anastomosis. United States: N. p., 2020. Web. doi:10.1371/journal.pone.0232165.
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Christley, Scott, Shogan, Benjamin, Levine, Zoe, Koo, Hyun, Guyton, Kristina, Owens, Sarah, Gilbert, Jack, Zaborina, Olga, & Alverdy, John C. Comparative genetics of Enterococcus faecalis intestinal tissue isolates before and after surgery in a rat model of colon anastomosis. United States. https://doi.org/10.1371/journal.pone.0232165
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Christley, Scott, Shogan, Benjamin, Levine, Zoe, Koo, Hyun, Guyton, Kristina, Owens, Sarah, Gilbert, Jack, Zaborina, Olga, and Alverdy, John C. Tue . "Comparative genetics of Enterococcus faecalis intestinal tissue isolates before and after surgery in a rat model of colon anastomosis". United States. https://doi.org/10.1371/journal.pone.0232165. https://www.osti.gov/servlets/purl/1668066.
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@article{osti_1668066,
title = {Comparative genetics of Enterococcus faecalis intestinal tissue isolates before and after surgery in a rat model of colon anastomosis},
author = {Christley, Scott and Shogan, Benjamin and Levine, Zoe and Koo, Hyun and Guyton, Kristina and Owens, Sarah and Gilbert, Jack and Zaborina, Olga and Alverdy, John C.},
abstractNote = {We have recently demonstrated that collagenolytic Enterococcus faecalis plays a key and causative role in the pathogenesis of anastomotic leak, an uncommon but potentially lethal complication characterized by disruption of the intestinal wound following segmental removal of the colon (resection) and its reconnection (anastomosis). Here we hypothesized that comparative genetic analysis of E. faecalis isolates present at the anastomotic wound site before and after surgery would shed insight into the mechanisms by which collagenolytic strains are selected for and predominate at sites of anastomotic disruption. Whole genome optical mapping of four pairs of isolates from rat colonic tissue obtained following surgical resection (herein named "pre-op" isolates) and then 6 days later from the anastomotic site (herein named "post-op" isolates) demonstrated that the isolates with higher collagenolytic activity formed a distinct cluster. In order to perform analysis at a deeper level, a single pair of E. faecalis isolates (16A pre-op and 16A post-op) was selected for whole genome sequencing and assembled using a hybrid assembly algorithm. Comparative genomics demonstrated absence of multiple gene clusters, notably a pathogenicity island in the post-op isolate. No differences were found in the fsr-gelE-sprE genes (EF1817-1822) responsible for regulation and production of collagenolytic activity. Analysis of unique genes among the 16A pre-op and post-op isolates revealed the predominance of transporter systems-related genes in the pre-op isolate and phage-related and hydrolytic enzyme-encoding genes in the post-op isolate. Despite genetic differences observed between pre-op and post-op isolates, the precise genetic determinants responsible for their differential expression of collagenolytic activity remains unknown.},
doi = {10.1371/journal.pone.0232165},
journal = {PLoS ONE},
number = 4,
volume = 15,
place = {United States},
year = {Tue Apr 28 00:00:00 EDT 2020},
month = {Tue Apr 28 00:00:00 EDT 2020}
}
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Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1371/journal.pone.0232165
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Figures / Tables:

Fig 1 Fig 1: Whole genome optical mapping of E. faecalis isolated from pre- and post-operative colonic tissues revealed distinct clustering of isolates with higher collagenolytic activity. (A), Collagenolytic activity of E. faecalis isolates based on the fluorescein-labeled gelatin degradation. n = 3, *p<0.01, by Student’s t-test. (B), Map similarity clusters basedmore » on the whole genome optical mapping. Optical mapping in silico sequences of reference strains was performed based on their whole genome sequences available from the GenBank database. (C), Optical maps. Blue-shaded regions between maps represent similar restriction pattern across the chromosome where vertical lines indicate the locations of restriction sites. Blue upside-down top hats represent insertions (Inst) and inverted grey features represent deletions (Dlt). Arrowed area represent polymorphic regions (Polymrph).« less
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