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Research Article | Host-Microbe Biology

A Distinct Contractile Injection System Gene Cluster Found in a Majority of Healthy Adult Human Microbiomes

Maria I. Rojas, Giselle S. Cavalcanti, Katelyn McNair, Sean Benler, Amanda T. Alker, Ana G. Cobián-Güemes, Melissa Giluso, Kyle Levi, Forest Rohwer, Barbara A. Bailey, Sinem Beyhan, Robert A. Edwards, Nicholas J. Shikuma
Jack A. Gilbert, Editor
Maria I. Rojas
aViral Information Institute, San Diego State University, San Diego, California, USA
bDepartment of Biology, San Diego State University, San Diego, California, USA
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  • ORCID record for Maria I. Rojas
Giselle S. Cavalcanti
aViral Information Institute, San Diego State University, San Diego, California, USA
bDepartment of Biology, San Diego State University, San Diego, California, USA
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Katelyn McNair
aViral Information Institute, San Diego State University, San Diego, California, USA
cComputational Science Research Center, San Diego State University, San Diego, California, USA
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Sean Benler
aViral Information Institute, San Diego State University, San Diego, California, USA
bDepartment of Biology, San Diego State University, San Diego, California, USA
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Amanda T. Alker
aViral Information Institute, San Diego State University, San Diego, California, USA
bDepartment of Biology, San Diego State University, San Diego, California, USA
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Ana G. Cobián-Güemes
aViral Information Institute, San Diego State University, San Diego, California, USA
bDepartment of Biology, San Diego State University, San Diego, California, USA
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Melissa Giluso
aViral Information Institute, San Diego State University, San Diego, California, USA
cComputational Science Research Center, San Diego State University, San Diego, California, USA
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Kyle Levi
aViral Information Institute, San Diego State University, San Diego, California, USA
cComputational Science Research Center, San Diego State University, San Diego, California, USA
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Forest Rohwer
aViral Information Institute, San Diego State University, San Diego, California, USA
bDepartment of Biology, San Diego State University, San Diego, California, USA
cComputational Science Research Center, San Diego State University, San Diego, California, USA
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Barbara A. Bailey
dDepartment of Mathematics and Statistics, San Diego State University, San Diego, California, USA
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Sinem Beyhan
bDepartment of Biology, San Diego State University, San Diego, California, USA
eDepartment of Infectious Diseases, J. Craig Venter Institute, La Jolla, California, USA
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Robert A. Edwards
aViral Information Institute, San Diego State University, San Diego, California, USA
bDepartment of Biology, San Diego State University, San Diego, California, USA
cComputational Science Research Center, San Diego State University, San Diego, California, USA
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Nicholas J. Shikuma
aViral Information Institute, San Diego State University, San Diego, California, USA
bDepartment of Biology, San Diego State University, San Diego, California, USA
cComputational Science Research Center, San Diego State University, San Diego, California, USA
eDepartment of Infectious Diseases, J. Craig Venter Institute, La Jolla, California, USA
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Jack A. Gilbert
University of California, San Diego
Roles: Editor
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DOI: 10.1128/mSystems.00648-20
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  • FIG 1
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    FIG 1

    Bacteroidales possess a distinct contractile injection system gene cluster. (A) Contractile injection systems are related to the contractile tails of bacteriophages. There are two main types of CIS; type 6 secretion systems (T6SS) are bound to the bacterial cell membrane and act from within the producing cell, while extracellular CIS (eCIS) are released by bacterial cell lysis and bind to target cells. (B) Unrooted phylogeny of CIS sheath protein sequences. A BIS group with a known subtype 4 T6SS and eCIS (orange) are distinct from organisms with known subtype 1, subtype 2 and subtype 3 T6SS (Table S1). Bacteria with BIS identified in this study are highlighted in red. Bootstrap values are expressed in numbers of occurrences that support the phylogenetic structure out of 100, from 1,000 resampling events.

  • FIG 2
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    FIG 2

    BIS gene clusters are found in three genetic architectures. (A and B) Synteny plot of BIS gene clusters in Bacteroides and Parabacteroides species (A) compared to those of P. luteoviolacea MACs, S. entomophila Afp, Photorhabdus PVCs, and “Ca. Amoebophilus asiaticus” subtype 4 T6SS (B). Representative CIS gene cluster architectures are shown, with genes color coded according to function. Genes with no significant sequence similarity at the amino acid level to any characterized proteins are light gray. Sequence coordinates of all gene clusters are provided in Table S3.

  • FIG 3
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    FIG 3

    BIS genes are abundant in human gut and mouth microbiomes and present in other human microbiomes. (A) Coverage plot of BIS genes (log10 of 1,000,000 · hits/reads) in 8,320 microbiomes associated with mucosal tissue, i.e., gut, mouth, nose, and other (includes vaginal and skin) tissues from 232 healthy humans. (B) Ten BIS genes are often found together in human metagenomes (cooccurrence network). Node size represents the number of hits for each protein across all runs. Line weight represents the number of times that any two proteins occurred together within a data set.

  • FIG 4
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    FIG 4

    BIS genes are expressed in vivo in humanized mice. Coverage plot of BIS genes (normalized by number of reads and protein nucleotide size) from 59 stool metatranscriptomes of humanized mouse microbiomes.

  • FIG 5
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    FIG 5

    BIS genes are present in the microbiomes of a majority (99%) of adult individuals from the United States and Europe. Frequencies of 18 BIS proteins from fecal samples of 338 individuals are shown. (A) HMP (n = 214) from healthy North American individuals (8); (B) MetaHIT (n = 124) from a study of European individuals (30). Protein hits are normalized by individual donor.

  • FIG 6
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    FIG 6

    BIS genes are present in higher abundance in healthy individuals than in individuals with IBD. (A) Percentages of individuals possessing a given number of BIS proteins from 214 healthy, 103 IBD, and 28 prediabetes fecal microbiome samples; (B) percentages of individuals possessing a given relative abundance (percentage) of Bacteroidetes within their gut microbiomes.

Tables

  • Figures
  • Supplemental Material
  • TABLE 1

    Statistical analyses of BIS protein counts and Bacteroidetes abundance confidence intervals for the difference in frequency medians between healthy, prediabetes, and IBD groups by a percentile nonparametric bootstrap methoda

    TABLE 1
    • ↵a The estimated difference in medians and the corresponding 95th-percentile confidence intervals (95% CI) are reported. Confidence intervals that do not cover zero have significantly different medians, denoted with an asterisk. See Table S5 in the supplemental material for asymptotic Wilcoxon rank sum test results.

Supplemental Material

  • Figures
  • Tables
  • TABLE S1

    Sequence similarity of sheath and tube proteins from representative secretion systems used to construct phylogenetic trees against BIS proteins. Download Table S1, DOCX file, 0.02 MB.

    Copyright © 2020 Rojas et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S1

    Unrooted phylogeny of CIS tube protein sequences. A BIS group with a known T6SS of subtype 4 and CIS (orange) are distinct from organisms with a known T6SS of subtype 1 and subtype 2 present in human pathogens and of a known subtype 3, characterized to mediate bacterium-bacterium interactions. Download FIG S1, EPS file, 1.9 MB.

    Copyright © 2020 Rojas et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S2

    Distinctive structural proteins (tube and sheath) representing diverse contractile injection systems. Download Table S2, DOCX file, 0.02 MB.

    Copyright © 2020 Rojas et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S3

    Sequence coordinates of genes within the BIS clusters that form three different genetic arrangements. Download Table S3, DOCX file, 0.02 MB.

    Copyright © 2020 Rojas et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S4

    Available annotations for the BIS gene cluster. Download Table S4, DOCX file, 0.01 MB.

    Copyright © 2020 Rojas et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S2

    BIS genes are expressed during in vitro culture of B. cellulosilyticus WH2. Relative abundances of RNA hits to 18 major genes of the BIS in a B. cellulosilyticus WH2 culture in MM supplemented with 31 different simple and complex carbohydrates. Download FIG S2, EPS file, 3.1 MB.

    Copyright © 2020 Rojas et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S3

    BIS protein abundance per individual in microbiomes of healthy, prediabetes, and IBD groups. Mean numbers of hits for each protein are normalized by gene size (nucleotides). Error bars indicate standard deviations from results for 214 healthy, 103 IBD, and 28 prediabetes individuals. Download FIG S3, EPS file, 1.2 MB.

    Copyright © 2020 Rojas et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S5

    Asymptotic Wilcoxon rank sum test results of the analyses of BIS protein counts and Bacteroidetes abundances. Download Table S5, DOCX file, 0.01 MB.

    Copyright © 2020 Rojas et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

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A Distinct Contractile Injection System Gene Cluster Found in a Majority of Healthy Adult Human Microbiomes
Maria I. Rojas, Giselle S. Cavalcanti, Katelyn McNair, Sean Benler, Amanda T. Alker, Ana G. Cobián-Güemes, Melissa Giluso, Kyle Levi, Forest Rohwer, Barbara A. Bailey, Sinem Beyhan, Robert A. Edwards, Nicholas J. Shikuma
mSystems Jul 2020, 5 (4) e00648-20; DOI: 10.1128/mSystems.00648-20

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A Distinct Contractile Injection System Gene Cluster Found in a Majority of Healthy Adult Human Microbiomes
Maria I. Rojas, Giselle S. Cavalcanti, Katelyn McNair, Sean Benler, Amanda T. Alker, Ana G. Cobián-Güemes, Melissa Giluso, Kyle Levi, Forest Rohwer, Barbara A. Bailey, Sinem Beyhan, Robert A. Edwards, Nicholas J. Shikuma
mSystems Jul 2020, 5 (4) e00648-20; DOI: 10.1128/mSystems.00648-20
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KEYWORDS

CIS
microbiome
secretion system
T6SS
bacteriophage
eCIS

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