Extensive horizontal gene transfer in cheese-associated bacteria

  1. Kevin S Bonham
  2. Benjamin E Wolfe
  3. Rachel J Dutton  Is a corresponding author
  1. University of California, San Diego, United States
  2. Tufts University, United States
  3. UC San Diego, United States

Abstract

Acquisition of genes through horizontal gene transfer (HGT) allows microbes to rapidly gain new capabilities and adapt to new or changing environments. Identifying widespread HGT regions within multispecies microbiomes can pinpoint the molecular mechanisms that play key roles in microbiome assembly. We sought to identify horizontally transferred genes within a model microbiome, the cheese rind. Comparing 31 newly-sequenced and 134 previously sequenced bacterial isolates from cheese rinds, we identified over 200 putative horizontally transferred genomic regions containing 4,844 protein coding genes. The largest of these regions are enriched for genes involved in siderophore acquisition, and are widely distributed in cheese rinds in both Europe and the US. These results suggest that horizontal gene transfer (HGT) is prevalent in cheese rind microbiomes, and the identification of genes that are frequently transferred in a particular environment may provide insight into the selective forces shaping microbial communities.

Data availability

The following data sets were generated
The following previously published data sets were used
    1. Wolfe BE
    2. Button JE
    3. Santarelli M
    4. Dutton RJ
    (2014) shotgun metagenomic data from cheese rinds used in Figure 4
    4524487.3, 4524500.3, 4524498.3, 4524496.3, 4524502.3, 4524495.3, 4524488.3, 4524490.3, 4524499.3, 4524497.3, 4524491.3, 4524493.3, 4524501.3, 4524482.3, 4524489.3, 4524483.3, 4524505.3, 4524494.3, 4524486.3, 4524504.3, 4524485.3, and 4524484.3.

Article and author information

Author details

  1. Kevin S Bonham

    Molecular Biology, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Benjamin E Wolfe

    Biology, Tufts University, Medford, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Rachel J Dutton

    Molecular Biology, UC San Diego, La Jolla, United States
    For correspondence
    rjdutton@ucsd.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2944-2182

Funding

National Institutes of Health (P50 GM068763)

  • Kevin S Bonham
  • Benjamin E Wolfe
  • Rachel J Dutton

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

Copyright

© 2017, Bonham et al.

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

  • 10,030
    views
  • 1,195
    downloads
  • 91
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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. Kevin S Bonham
  2. Benjamin E Wolfe
  3. Rachel J Dutton
(2017)
Extensive horizontal gene transfer in cheese-associated bacteria
eLife 6:e22144.
https://doi.org/10.7554/eLife.22144

Share this article

https://doi.org/10.7554/eLife.22144

Further reading

    1. Developmental Biology
    2. Genetics and Genomics
    Debashish U Menon, Prabuddha Chakraborty ... Terry Magnuson
    Research Article

    We present evidence implicating the BAF (BRG1/BRM Associated Factor) chromatin remodeler in meiotic sex chromosome inactivation (MSCI). By immunofluorescence (IF), the putative BAF DNA binding subunit, ARID1A (AT-rich Interaction Domain 1 a), appeared enriched on the male sex chromosomes during diplonema of meiosis I. Germ cells showing a Cre-induced loss of ARID1A arrested in pachynema and failed to repress sex-linked genes, indicating a defective MSCI. Mutant sex chromosomes displayed an abnormal presence of elongating RNA polymerase II coupled with an overall increase in chromatin accessibility detectable by ATAC-seq. We identified a role for ARID1A in promoting the preferential enrichment of the histone variant, H3.3, on the sex chromosomes, a known hallmark of MSCI. Without ARID1A, the sex chromosomes appeared depleted of H3.3 at levels resembling autosomes. Higher resolution analyses by CUT&RUN revealed shifts in sex-linked H3.3 associations from discrete intergenic sites and broader gene-body domains to promoters in response to the loss of ARID1A. Several sex-linked sites displayed ectopic H3.3 occupancy that did not co-localize with DMC1 (DNA meiotic recombinase 1). This observation suggests a requirement for ARID1A in DMC1 localization to the asynapsed sex chromatids. We conclude that ARID1A-directed H3.3 localization influences meiotic sex chromosome gene regulation and DNA repair.

    1. Genetics and Genomics
    2. Immunology and Inflammation
    Stephanie Guillet, Tomi Lazarov ... Frédéric Geissmann
    Research Article

    Systemic lupus erythematosus (SLE) is an autoimmune disease, the pathophysiology and genetic basis of which are incompletely understood. Using a forward genetic screen in multiplex families with SLE, we identified an association between SLE and compound heterozygous deleterious variants in the non-receptor tyrosine kinases (NRTKs) ACK1 and BRK. Experimental blockade of ACK1 or BRK increased circulating autoantibodies in vivo in mice and exacerbated glomerular IgG deposits in an SLE mouse model. Mechanistically, NRTKs regulate activation, migration, and proliferation of immune cells. We found that the patients’ ACK1 and BRK variants impair efferocytosis, the MERTK-mediated anti-inflammatory response to apoptotic cells, in human induced pluripotent stem cell (hiPSC)-derived macrophages, which may contribute to SLE pathogenesis. Overall, our data suggest that ACK1 and BRK deficiencies are associated with human SLE and impair efferocytosis in macrophages.