Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Bacterial vampirism mediated through taxis to serum

Journal Article · · eLife
DOI:https://doi.org/10.7554/elife.93178· OSTI ID:2471019
Bacteria of the family Enterobacteriaceae are associated with gastrointestinal (GI) bleeding and bacteremia and are a leading cause of death, from sepsis, for individuals with inflammatory bowel diseases. The bacterial behaviors and mechanisms underlying why these bacteria are prone to bloodstream entry remain poorly understood. Herein, we report that clinical isolates of non-typhoidal Salmonella enterica serovars, Escherichia coli, and Citrobacter koseri are rapidly attracted toward sources of human serum. To simulate GI bleeding, we utilized an injection-based microfluidics device and found that femtoliter volumes of human serum are sufficient to induce bacterial attraction to the serum source. This response is orchestrated through chemotaxis and the chemoattractant L-serine, an amino acid abundant in serum that is recognized through direct binding by the chemoreceptor Tsr. We report the first crystal structures of Salmonella Typhimurium Tsr in complex with L-serine and identify a conserved amino acid recognition motif for L-serine shared among Tsr orthologues. We find Tsr to be widely conserved among Enterobacteriaceae and numerous World Health Organization priority pathogens associated with bloodstream infections. Lastly, we find that Enterobacteriaceae use human serum as a source of nutrients for growth and that chemotaxis and the chemoreceptor Tsr provide a competitive advantage for migration into enterohemorrhagic lesions. We define this bacterial behavior of taxis toward serum, colonization of hemorrhagic lesions, and the consumption of serum nutrients as ‘bacterial vampirism’, which may relate to the proclivity of Enterobacteriaceae for bloodstream infections.
Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). Advanced Light Source (ALS)
Sponsoring Organization:
National Institute of Allergy and Infectious Diseases (NIAID); National Institute of General Medical Sciences (NIGMS); National Institutes of Health (NIH); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
2471019
Journal Information:
eLife, Journal Name: eLife Vol. 12; ISSN 2050-084X
Publisher:
eLife Sciences Publications, Ltd.Copyright Statement
Country of Publication:
United States
Language:
English

References (71)

Decreased Serum Levels of D-Serine in Patients With Schizophrenia journal June 2003
The microbiome in wound repair and tissue fibrosis journal November 2012
DIALS as a toolkit journal November 2021
Microbiome and Gut Dysbiosis book January 2018
Serum amino acid concentrations in aging men and women journal June 2003
The norepinephrine tissue concentration and neuropeptide Y immunoreactivity in genitourinary organs of the spontaneously hypertensive rat journal January 1996
Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis journal February 2022
Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis journal March 2018
The mortality rate among patients with acute upper GI bleeding (with/without EGD) at Aleppo University Hospital: A retrospective study journal November 2021
Molecular Mechanism for Attractant Signaling to DHMA by E. coli Tsr journal January 2020
Chemodetection and Destruction of Host Urea Allows Helicobacter pylori to Locate the Epithelium journal August 2015
The combination of CRISPR-MVLST and PFGE provides increased discriminatory power for differentiating human clinical isolates of Salmonella enterica subsp. enterica serovar Enteritidis journal May 2013
Oxygen as a driver of gut dysbiosis journal April 2017
Diversity of bacterial chemosensory systems journal June 2021
The pig: a model for human infectious diseases journal January 2012
Bacterial chemotaxis in human diseases journal May 2023
Pharmacokinetics of oral l-serine supplementation in a single patient journal September 2020
Mechanisms of inflammation-driven bacterial dysbiosis in the gut journal January 2017
Gut inflammation provides a respiratory electron acceptor for Salmonella journal September 2010
NIH Image to ImageJ: 25 years of image analysis journal June 2012
Molecular mechanisms of Escherichia coli pathogenicity journal December 2009
Gut biogeography of the bacterial microbiota journal October 2015
Chemotaxis of Escherichia coli to major hormones and polyamines present in human gut journal July 2018
Glycine, serine and threonine metabolism confounds efficacy of complement-mediated killing journal July 2019
Complete structure of the chemosensory array core signalling unit in an E. coli minicell strain journal February 2020
Dietary l-serine confers a competitive fitness advantage to Enterobacteriaceae in the inflamed gut journal November 2019
Bacterial motility: machinery and mechanisms journal September 2021
The ecological roles of bacterial chemotaxis journal March 2022
Nutritional immunity: the battle for nutrient metals at the host–pathogen interface journal May 2022
Structure and dynamics of the E. coli chemotaxis core signaling complex by cryo-electron tomography and molecular simulations journal January 2020
P130 Leading Causes of Mortality in Inflammatory Bowel Disease: a Nationwide Analysis journal February 2020
Ligand Specificity Determined by Differentially Arranged Common Ligand-binding Residues in Bacterial Amino Acid Chemoreceptors Tsr and Tar journal October 2011
Toll-like Receptor 11 (TLR11) Prevents Salmonella Penetration into the Murine Peyer Patches journal December 2012
Characteristics of Campylobacter and Salmonella Infections and Acute Gastroenteritis in Older Adults in Australia, Canada, and the United States journal January 2019
A catalogue of signal molecules that interact with sensor kinases, chemoreceptors and transcriptional regulators journal August 2021
The effect of bacterial chemotaxis on host infection and pathogenicity journal October 2017
P129 Inpatient Outcomes of Sepsis in Inflammatory Bowel Disease Patients: a 2016 Nationwide Inpatient Sample Analysis journal January 2020
MolProbity: all-atom contacts and structure validation for proteins and nucleic acids journal May 2007
Reference collection of strains of the Salmonella typhimurium complex from natural populations journal March 1991
Coot model-building tools for molecular graphics journal November 2004
PHENIX: a comprehensive Python-based system for macromolecular structure solution journal January 2010
Overview of the CCP 4 suite and current developments journal March 2011
Targeting motility and chemotaxis as a strategy to combat bacterial pathogens journal June 2023
Motility allows S. Typhimurium to benefit from the mucosal defence journal May 2008
Linking Crystallographic Model and Data Quality journal May 2012
Worldwide Epidemiology ofSalmonellaSerovars in Animal-Based Foods: a Meta-analysis journal July 2019
The Host Cellular Immune Response to Infection by Campylobacter Spp. and Its Role in Disease journal July 2021
Helicobacter pylori Uses the TlpB Receptor To Sense Sites of Gastric Injury journal September 2019
Identification of a Putative Salmonella enterica Serotype Typhimurium Host Range Factor with Homology to IpaH and YopM by Signature-Tagged Mutagenesis journal December 1999
Chemotaxis of Escherichia coli to Norepinephrine (NE) Requires Conversion of NE to 3,4-Dihydroxymandelic Acid journal December 2014
Subtyping of Salmonella enterica Serovar Newport Outbreak Isolates by CRISPR-MVLST and Determination of the Relationship between CRISPR-MVLST and PFGE Results journal May 2013
Salmonella versus the Microbiome journal February 2021
ChePep Controls Helicobacter pylori Infection of the Gastric Glands and Chemotaxis in the Epsilonproteobacteria journal September 2011
Energy Taxis toward Host-Derived Nitrate Supports a Salmonella Pathogenicity Island 1-Independent Mechanism of Invasion journal September 2016
Modernized Tools for Streamlined Genetic Manipulation and Comparative Study of Wild and Diverse Proteobacterial Lineages journal October 2018
Risk of common infections in people with inflammatory bowel disease in primary care: a population-based cohort study journal February 2021
Survival Impact and Clinical Predictors of Acute Gastrointestinal Bleeding in Patients With Bloodstream Infection journal November 2019
Risk of bacteremia in hospitalised patients with inflammatory bowel disease: a 9‐year cohort study journal March 2020
Risk factors for mortality among patients admitted with upper gastrointestinal bleeding at a tertiary hospital: a prospective cohort study journal December 2017
Helicobacter pylori senses bleach (HOCl) as a chemoattractant using a cytosolic chemoreceptor journal August 2019
Impact of Cytochrome P450 2D6 Function on the Chiral Blood Plasma Pharmacokinetics of 3,4-Methylenedioxymethamphetamine (MDMA) and Its Phase I and II Metabolites in Humans journal March 2016
Salmonella Uses Energy Taxis to Benefit from Intestinal Inflammation journal April 2013
Motility and Chemotaxis Mediate the Preferential Colonization of Gastric Injury Sites by Helicobacter pylori journal July 2014
Multiple Acid Sensors Control Helicobacter pylori Colonization of the Stomach journal January 2017
Defensins: A Double-Edged Sword in Host Immunity journal May 2020
Serum Serine and the Risk of All-Cause Mortality: A Nested Case-Control Study From the China Stroke Primary Prevention Trial (CSPPT) journal July 2022
Investigating Intestinal Inflammation in DSS-induced Model of IBD journal February 2012
Diagnosis of gastrointestinal bleeding: A practical guide for clinicians journal January 2014
Plasma Levels of Norepinephrine journal May 1978
CryoEM and computer simulations reveal a novel kinase conformational switch in bacterial chemotaxis signaling journal November 2015
Severe Sepsis Caused by Bacteria That Entered via the Intestinal Tract: A Case of Crohn's Disease in a Child journal August 2020

Similar Records

Evolutionary genomics suggests that CheV is an additional adaptor for accommodating specific chemoreceptors within the chemotaxis signaling complex
Journal Article · Wed Feb 03 19:00:00 EST 2016 · PLoS Computational Biology (Online) · OSTI ID:1327747

The Azospirillum brasilense Core Chemotaxis Proteins CheA1 and CheA4 Link Chemotaxis Signaling with Nitrogen Metabolism
Journal Article · Mon Feb 15 19:00:00 EST 2021 · mSystems · OSTI ID:1767841

Metabolites from intact phage-infected Synechococcus chemotactically attract heterotrophic marine bacteria
Journal Article · Sat Nov 30 19:00:00 EST 2024 · Nature Microbiology · OSTI ID:2573003

Related Subjects