Title | Bacterial Swarmers Enriched During Intestinal Stress Ameliorate Damage. |
Publication Type | Journal Article |
Year of Publication | 2021 |
Authors | De A, Chen W, Li H, Wright JR, Lamendella R, Lukin DJ, Szymczak WA, Sun K, Kelly L, Ghosh S, Kearns DB, He Z, Jobin C, Luo X, Byju A, Chatterjee S, San Yeoh B, Vijay-Kumar M, Tang JX, Prajapati M, Bartnikas TB, Mani S |
Journal | Gastroenterology |
Volume | 161 |
Issue | 1 |
Pagination | 211-224 |
Date Published | 2021 07 |
ISSN | 1528-0012 |
Keywords | Adult, Aged, Aged, 80 and over, Animals, Bacteriological Techniques, Colitis, Disease Models, Animal, Dysbiosis, Enterobacter, Feces, Female, Gastrointestinal Microbiome, Humans, Inflammatory Bowel Diseases, Intestinal Mucosa, Male, Mice, Mice, Inbred C57BL, Microbial Viability, Middle Aged, Movement, Probiotics, Re-Epithelialization, Wound Healing, Young Adult |
Abstract | BACKGROUND AND AIMS: Bacterial swarming, a collective movement on a surface, has rarely been associated with human pathophysiology. This study aims to define a role for bacterial swarmers in amelioration of intestinal stress. METHODS: We developed a polymicrobial plate agar assay to detect swarming and screened mice and humans with intestinal stress and inflammation. From chemically induced colitis in mice, as well as humans with inflammatory bowel disease, we developed techniques to isolate the dominant swarmers. We developed swarm-deficient but growth and swim-competent mutant bacteria as isogenic controls. We performed bacterial reinoculation studies in mice with colitis, fecal 16S, and meta-transcriptomic analyses, as well as in vitro microbial interaction studies. RESULTS: We show that bacterial swarmers are highly predictive of intestinal stress in mice and humans. We isolated a novel Enterobacter swarming strain, SM3, from mouse feces. SM3 and other known commensal swarmers, in contrast to their mutant strains, abrogated intestinal inflammation in mice. Treatment of colitic mice with SM3, but not its mutants, enriched beneficial fecal anaerobes belonging to the family of Bacteroidales S24-7. We observed SM3 swarming associated pathways in the in vivo fecal meta-transcriptomes. In vitro growth of S24-7 was enriched in presence of SM3 or its mutants; however, because SM3, but not mutants, induced S24-7 in vivo, we concluded that swarming plays an essential role in disseminating SM3 in vivo. CONCLUSIONS: Overall, our work identified a new but counterintuitive paradigm in which intestinal stress allows for the emergence of swarming bacteria; however, these bacteria act to heal intestinal inflammation. |
DOI | 10.1053/j.gastro.2021.03.017 |
Alternate Journal | Gastroenterology |
PubMed ID | 33741315 |
PubMed Central ID | PMC8601393 |
Grant List | R01 GM135218 / GM / NIGMS NIH HHS / United States R01 ES030197 / ES / NIEHS NIH HHS / United States R01 CA127231 / CA / NCI NIH HHS / United States R01 CA161879 / CA / NCI NIH HHS / United States UL1 TR001073 / TR / NCATS NIH HHS / United States S10 RR029398 / RR / NCRR NIH HHS / United States S10 OD019961 / OD / NIH HHS / United States R01 CA222469 / CA / NCI NIH HHS / United States P30 CA013330 / CA / NCI NIH HHS / United States |