1. Microbiology and Infectious Disease
  2. Physics of Living Systems

Gut bacterial aggregates as living gels

  1. Brandon H Schlomann
  2. Raghuveer Parthasarathy  Is a corresponding author
  1. University of Oregon, United States
https://doi.org/10.7554/eLife.71105
Share this article
Cite this article
  1. Brandon H Schlomann
  2. Raghuveer Parthasarathy
(2021)
Gut bacterial aggregates as living gels
eLife 10:e71105.
https://doi.org/10.7554/eLife.71105
  2. Download BibTeX
  3. Download .RIS

Abstract

The spatial organization of gut microbiota influences both microbial abundances and host-microbe interactions, but the underlying rules relating bacterial dynamics to large-scale structure remain unclear. To this end we studied experimentally and theoretically the formation of three-dimensional bacterial clusters, a key parameter controlling susceptibility to intestinal transport and access to the epithelium. Inspired by models of structure formation in soft materials, we sought to understand how the distribution of gut bacterial cluster sizes emerges from bacterial-scale kinetics. Analyzing imaging-derived data on cluster sizes for eight different bacterial strains in the larval zebrafish gut, we find a common family of size distributions that decay approximately as power laws with exponents close to -2, becoming shallower for large clusters in a strain-dependent manner. We show that this type of distribution arises naturally from a Yule-Simons-type process in which bacteria grow within clusters and can escape from them, coupled to an aggregation process that tends to condense the system toward a single massive cluster, reminiscent of gel formation. Together, these results point to the existence of general, biophysical principles governing the spatial organization of the gut microbiome that may be useful for inferring fast-timescale dynamics that are experimentally inaccessible.

Data availability

A table of all bacterial cluster sizes analysed in this study is included in the Supplementary Data File. MATLAB code for simulating the models described in the study is available at https://github.com/rplab/cluster_kinetics

The following previously published data sets were used

Article and author information

Author details

  1. Brandon H Schlomann

    University of Oregon, Eugene, United States
    Competing interests
    The authors declare that no competing interests exist.

  2. Raghuveer Parthasarathy

    University of Oregon, Eugene, United States
    For correspondence
    raghu@uoregon.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6006-4749

Funding

National Institutes of Health (P50GM09891)

  • Brandon H Schlomann
  • Raghuveer Parthasarathy

National Institutes of Health (P01GM125576)

  • Brandon H Schlomann
  • Raghuveer Parthasarathy

National Institutes of Health (F32AI112094)

  • Brandon H Schlomann
  • Raghuveer Parthasarathy

National Institutes of Health (T32GM007759)

  • Raghuveer Parthasarathy

National Science Foundation (1427957)

  • Brandon H Schlomann
  • Raghuveer Parthasarathy

James S. McDonnell Foundation

  • Brandon H Schlomann

Kavli Foundation (Kavli Microbiome Ideas Challenge)

  • Brandon H Schlomann
  • Raghuveer Parthasarathy

National Institutes of Health (P01HD22486)

  • Brandon H Schlomann
  • Raghuveer Parthasarathy

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: The studies that generated the data analyzed in this paper (see cited references) were done in strict accordance with protocols approved by the University of Oregon Institutional Animal Care and Use Committee and following standard protocols.

Reviewing Editor

  1. Kevin B Wood, University of Michigan, United States

Publication history

  1. Preprint posted: June 8, 2021 (view preprint)
  2. Received: June 9, 2021
  3. Accepted: September 6, 2021
  4. Accepted Manuscript published: September 7, 2021 (version 1)
  5. Version of Record published: October 13, 2021 (version 2)
  6. Version of Record updated: October 22, 2021 (version 3)
  7. Version of Record updated: October 25, 2021 (version 4)

Copyright

© 2021, Schlomann & Parthasarathy

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,334
    Page views
  • 211
    Downloads
  • 2
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Brandon H Schlomann
  2. Raghuveer Parthasarathy
(2021)
Gut bacterial aggregates as living gels
eLife 10:e71105.
https://doi.org/10.7554/eLife.71105

Categories and tags

Research organism

Further reading

    1. Cancer Biology
    2. Microbiology and Infectious Disease

    Evidence for virus-mediated oncogenesis in bladder cancers arising in solid organ transplant recipients

    Gabriel J Starrett, Kelly Yu ... Eric A Engels
    Research Article

    A small percentage of bladder cancers in the general population have been found to harbor DNA viruses. In contrast, up to 25% of tumors of solid organ transplant recipients, who are at an increased risk of developing bladder cancer and have overall poorer outcome, harbor BK polyomavirus (BKPyV). To better understand the biology of the tumors and the mechanisms of carcinogenesis from potential oncoviruses, we performed whole genome and transcriptome sequencing on bladder cancer specimens from 43 transplant patients. Nearly half of tumors from this patient population contained viral sequences. The most common were from BKPyV (N=9, 21%), JC polyomavirus (N=7, 16%), carcinogenic human papillomaviruses (N=3, 7%), and torque teno viruses (N=5, 12%). Immunohistochemistry revealed variable Large T antigen expression in BKPyV-positive tumors ranging from 100% positive staining of tumor tissue to less than 1%. In most cases of BKPyV-positive tumors, the viral genome appeared to be clonally integrated into the host chromosome consistent with microhomology-mediated end joining and coincided with focal amplifications of the tumor genome similar to other virus-mediated cancers. Significant changes in host gene expression consistent with the functions of BKPyV Large T antigen were also observed in these tumors. Lastly, we identified four mutation signatures in our cases with those attributable to APOBEC3 and SBS5 being the most abundant. Mutation signatures associated with the antiviral drug, ganciclovir, and aristolochic acid, a nephrotoxic compound found in some herbal medicines, were also observed. The results suggest multiple pathways to carcinogenesis in solid organ transplant recipients with a large fraction being virus-associated.

    1. Genetics and Genomics
    2. Microbiology and Infectious Disease

    Enterobacterales plasmid sharing amongst human bloodstream infections, livestock, wastewater, and waterway niches in Oxfordshire, UK

    William Matlock, Samuel Lipworth ... REHAB Consortium
    Research Article

    Plasmids enable the dissemination of antimicrobial resistance (AMR) in common Enterobacterales pathogens, representing a major public health challenge. However, the extent of plasmid sharing and evolution between Enterobacterales causing human infections and other niches remains unclear, including the emergence of resistance plasmids. Dense, unselected sampling is highly relevant to developing our understanding of plasmid epidemiology and designing appropriate interventions to limit the emergence and dissemination of plasmid-associated AMR. We established a geographically and temporally restricted collection of human bloodstream infection (BSI)-associated, livestock-associated (cattle, pig, poultry, and sheep faeces, farm soils) and wastewater treatment work (WwTW)-associated (influent, effluent, waterways upstream/downstream of effluent outlets) Enterobacterales. Isolates were collected between 2008-2020 from sites <60km apart in Oxfordshire, UK. Pangenome analysis of plasmid clusters revealed shared 'backbones', with phylogenies suggesting an intertwined ecology where well-conserved plasmid backbones carry diverse accessory functions, including AMR genes. Many plasmid 'backbones' were seen across species and niches, raising the possibility that plasmid movement between these followed by rapid accessory gene change could be relatively common. Overall, the signature of identical plasmid sharing is likely to be a highly transient one, implying that plasmid movement might be occurring at greater rates than previously estimated, raising a challenge for future genomic One Health studies.

    1. Microbiology and Infectious Disease

    Viral Replication: Learning more about hepatitis E virus

    Altaira D Dearborn, Ashish Kumar, Joseph Marcotrigiano
    Insight

    A domain in the ORF1 polyprotein of the hepatitis E virus that was previously thought to be a protease is actually a zinc-binding domain.