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PreprintCited by 14Bacterial Genetics and BiotechnologyBiochemical and Structural CharacterizationMicrobial Community Ecology and Physiology

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Saccharibacteria deploy two distinct Type IV pili, driving episymbiosis, host competition, and twitching motility

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Grossman, Alex S., Lei, Lei, Botting, Jack M., Liu, Jett, Nahar, Nusrat, Souza, João Gabriel S., Liu, Jun, McLean, Jeffrey S., He, Xuesong, Bor, Batbileg·2024·The ISME Journal
DOI 10.1101/2024.11.25.624915PMC PMC12206443

Preprint — published as 10.1093/ismejo/wraf119 · Paper page

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Abstract

All cultivated Patescibacteria, or CPR, exist as obligate episymbionts on other microbes. Despite being ubiquitous in mammals and environmentally, molecular mechanisms of host identification and binding amongst ultrasmall bacterial episymbionts are largely unknown. Type 4 pili (T4P) are well conserved in this group and predicted to facilitate symbiotic interactions. To test this, we targeted T4P pilin genes in Saccharibacteria Nanosynbacter lyticus strain TM7x to assess their essentiality and roles in symbiosis. Our results revealed that N. lyticus assembles two distinct T4P, a non-essential thin pili that has the smallest diameter of any T4P and contributes to host-binding, episymbiont growth, and competitive fitness relative to other Saccharibacteria, and an essential thick pili whose functions include twitching motility. Identification of lectin-like minor pilins and modification of host cell walls suggest glycan binding mechanisms. Collectively our findings demonstrate that Saccharibacteria encode unique extracellular pili that are vital mediators of their underexplored episymbiotic lifestyle.

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  1. 10.1073/pnas.0704662104 · DOI
  2. 10.1038/nature12352 · DOI · Paper page
  3. 10.1038/nature14486 · DOI · Paper page
  4. 10.1038/s41564-020-00840-5 · DOI
  5. 10.1186/s40168-017-0331-1 · DOI
  6. 10.1038/s41564-017-0012-7 · DOI · Paper page
  7. 10.1186/s40168-017-0360-9 · DOI
  8. 10.1038/nmicrobiol.2016.48 · DOI · Paper page
  9. 10.1016/j.cell.2018.02.016 · DOI · Paper page
  10. 10.1038/s41587-019-0260-6 · DOI
  11. 10.1073/pnas.1419038112 · DOI
  12. 10.1128/mbio.01711-22 · DOI
  13. 10.1016/j.syapm.2013.08.007 · DOI
  14. 10.1177/0022034519831671 · DOI
  15. 10.1038/s41564-021-00892-1 · DOI
  16. 10.1073/pnas.2215990119 · DOI
  17. 10.1007/s12275-008-0249-1 · DOI
  18. 10.7717/peerj.8614 · DOI
  19. 10.1128/mbio.00521-21 · DOI
  20. 10.1128/JB.00542-10 · DOI · Paper page
  21. Naud, S. et al. Preliminary landscape of Candidatus Saccharibacteria in the human microbiome. Front Cell Infect Microbiol 13, (2023). · DOI
  22. 10.1016/j.celrep.2020.107939 · DOI
  23. 10.1371/journal.pone.0037919 · DOI · Paper page
  24. 10.1098/rstb.2013.0376 · DOI
  25. 10.1038/ng.2906 · DOI · Paper page
  26. 10.1038/nature21674 · DOI
  27. 10.1073/pnas.2021655118 · DOI
  28. 10.1016/j.cub.2017.10.040 · DOI
  29. 10.1038/s41586-022-05620-1 · DOI · Paper page
  30. 10.1073/pnas.2319790121 · DOI
  31. 2022, Strain-Level Variation and Diverse Host Bacterial Responses in Episymbiotic Saccharibacteria, mSystems, 7, e01488
  32. 2022, Transcriptome of Epibiont Saccharibacteria Nanosynbacter lyticus Strain TM7x During the Establishment of Symbiosis, J Bacteriol, 204, e00112
  33. 10.1093/ismejo/wrad034 · DOI
  34. 10.1073/pnas.2114909119 · DOI
  35. 10.1016/j.cell.2023.08.017 · DOI · Paper page
  36. 10.1038/s41467-019-12171-z · DOI
  37. 10.1038/s41579-019-0195-4 · DOI
  38. 10.1128/MMBR.00035-12 · DOI
  39. 10.1016/j.jmb.2009.09.034 · DOI
  40. 10.1111/j.1365-2958.2006.05341.x · DOI
  41. 2023, Systematic functional analysis of the Com pilus in Streptococcus sanguinis: a minimalistic type 4 filament dedicated to DNA uptake in monoderm bacteria, mBio, 15, e02667
  42. Pelicic, V . Mechanism of assembly of type 4 filaments: everything you always wanted to know (but were afraid to ask). Microbiology (N Y) 169, (2023). · DOI
  43. 10.1371/journal.pbio.3000390 · DOI
  44. 10.1006/jmbi.1990.9999 · DOI · Paper page
  45. 10.1093/nar/25.17.3389 · DOI · Paper page
  46. 10.1007/978-1-0716-3445-5_1 · DOI
  47. 10.1093/NAR/GKAB1061 · DOI · Paper page
  48. 10.1128/mbio.00131-10 · DOI
  49. 10.1073/pnas.1810625115 · DOI
  50. 10.1038/s41587 · DOI
  51. 10.1038/378032a0 · DOI
  52. 10.1007/s00430-019-00642-5 · DOI
  53. 10.1093/nar/gkac1096 · DOI · Paper page
  54. 10.1038/s41467-020-18803-z · DOI
  55. 10.1128/JB.01793-07 · DOI
  56. 10.1073/pnas.0402397101 · DOI
  57. 10.1111/j.1365-2958.2007.05806.x · DOI
  58. 10.1093/nar/gkae410 · DOI
  59. 10.1371/journal.pone.0040155 · DOI
  60. 10.1038/s41467-022-33564-7 · DOI
  61. 10.1128/IAI.70.1.1-4.2002 · DOI
  62. 2021, Fresh extension of Vibrio cholerae competence Type IV pili predisposes them for motor-independent retraction, Appl Environ Microbiol, 87, e00478
  63. 10.1128/microbiolspec.psib-0011–2018 · DOI
  64. 10.1038/ismej.2014.60 · DOI
  65. 10.1177/0022034520905792 · DOI
  66. 2008, The bundlin pilin protein of enteropathogenic Escherichia coli is an N-acetyllactosamine-specific lectin, Cell Microbiol, 10, 177
  67. 10.1172/JCI116779 · DOI
  68. 10.1073/pnas.2216237120 · DOI · Paper page
  69. 10.1128/JB.01942-06 · DOI
  70. 10.1002/pro.4519 · DOI
  71. 10.1093/nar/gkac387 · DOI
  72. 10.1016/S0021-9258(18)86371-2 · DOI
  73. 10.1074/jbc.M115.693473 · DOI
  74. 10.1371/journal.pone.0029629 · DOI
  75. 10.1073/pnas.0911616107 · DOI
  76. 10.1128/mbio.01303-17 · DOI
  77. Guérin, H. et al. Molecular mechanisms underlying the structural diversity of rhamnose-rich cell wall polysaccharides in lactococci. Journal of Biological Chemistry 300, (2024). · DOI
  78. Guérin, H. , Kulakauskas, S. & Chapot-Chartier, M.-P . Structural variations and roles of rhamnose-rich cell wall polysaccharides in Gram-positive bacteria. Journal of Biological Chemistry 298, (2022). · DOI
  79. 10.1074/jbc.M112.446963 · DOI
  80. Mücke, P.-A. , Ostrzinski, A. , Hammerschmidt, S. , Maaß, S. & Becher, D . Proteomic adaptation of Streptococcus pneumoniae to the antimicrobial peptide Human Beta Defensin 3 (hBD3) in comparison to other cell surface stresses. Microorganisms 8, (2020). · DOI
  81. 10.1134/S0026261721030139 · DOI
  82. 10.1111/mmi.14330 · DOI
  83. 10.1038/s41589-021-00803-9 · DOI
  84. 10.1111/j.2041-1014.2010.00593.x · DOI
  85. 10.1128/AEM.02985-06 · DOI
  86. 10.1007/s00248-015-0711-7 · DOI
  87. 10.1038/s41396-020-00736-6 · DOI
  88. 10.1038/nrgastro.2017.173 · DOI · Paper page
  89. 10.1146/annurev.micro.60.080805.142106 · DOI
  90. 10.1038/s41467-020-15650-w · DOI
  91. 10.1111/j.1574-6968.2006.00438.x · DOI
  92. 10.1101/2023.07.17.549387 · DOI
  93. 2021, Type IV pili of Streptococcus sanguinis contribute to pathogenesis in experimental infective endocarditis, Microbiol Spectr, 9, e01752
  94. 10.1128/JB.00396-09 · DOI
  95. 10.1073/pnas.2321989121 · DOI
  96. 10.1073/pnas.242523299 · DOI
  97. 10.1371/journal.pbio.0060087 · DOI
  98. 10.1073/pnas.1720071115 · DOI
  99. 10.1128/iai.00943-17 · DOI
  100. 10.1038/s41467-023-42872-5 · DOI · Paper page
  101. 10.1128/IAI.73.12.7922-7931.2005 · DOI
  102. 2018, Pseudomonas aeruginosa defends against phages through type IV pilus glycosylation, Nat Microbiol, 3, 47
  103. 10.1007/s00430-019-00642-5 · DOI
  104. 10.1134/S0006297920030128 · DOI
  105. 10.2323/jgam.36.255 · DOI
  106. 10.1093/bioinformatics/btac672 · DOI
  107. 10.1371/journal.pcbi.1002195 · DOI · Paper page
  108. Criscuolo, A. & Gribaldo, S . BMGE (Block Mapping and Gathering with Entropy): A new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol 10, 210 (2010). · DOI
  109. 10.1093/molbev/msaa015 · DOI · Paper page
  110. 10.1093/sysbio/sys062 · DOI
  111. 10.1038/nmeth.4285 · DOI · Paper page
  112. 10.1093/molbev/msn067 · DOI · Paper page
  113. 10.1371/journal.pone.0028919 · DOI
  114. 2022, Exploitation of a bacterium-encoded lytic transglycosylase by a human oral lytic phage to facilitate infection, J Virol, 96, e01063
  115. 10.1016/j.jsb.2016.07.011 · DOI
  116. 10.1038/nmeth.4193 · DOI
  117. 10.1006/jsbi.1996.0013 · DOI
  118. 10.1038/nmeth.2019 · DOI · Paper page
  119. Schrodinger LLC. The PyMOL Molecular Graphics System, Version 1.8. Preprint at (2015).
  120. 10.1093/bioinformatics/btae370 · DOI
  121. 10.1093/bioinformatics/btg1086 · DOI
  122. Bedree, J. K. et al. Quorum sensing modulates the epibiotic-parasitic relationship between Actinomyces odontolyticus and its Saccharibacteria epibiont, a Nanosynbacter lyticus strain, TM7x. Front Microbiol 9, (2018). · DOI
  123. 10.1101/2024.07.17.604004 · DOI
  124. 10.1111/mmi.12780 · DOI
  125. 10.1128/jb.176.3.733-747.1994 · DOI
  126. 2023, Development of a xylose-inducible promoter and riboswitch combination system for manipulating gene expression in Fusobacterium nucleatum, Appl Environ Microbiol, 89, e00667
  127. 10.1128/IAI.66.3.1159-1166.1998 · DOI
  128. 10.1128/JB.00476-06 · DOI
  129. 10.1073/pnas.1522149113 · DOI · Paper page
  130. 10.1016/j.chom.2021.09.009 · DOI

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Metadata

Authors
Grossman, A. S., Lei, L., Botting, J. M., Liu, J., Nahar, N., Souza, J. G. S., Liu, J., McLean, J. S., He, X., & Bor, B.
Affiliations
  • The Forsyth Institute (US)
  • Sichuan University (CN)
  • Yale University (US)
  • University of Washington (US)
Corresponding author
Bor, Batbileg
ORCID
Venue
The ISME Journal
Publisher
openRxiv
Published
2024-11-25
Volume
19
Issue
1
ISSN
1751-7362 (ISSN-L)
DOI
10.1101/2024.11.25.624915
PMC
PMC12206443
OpenAlex
W4411134751
Cited by
14
References
135
Citations by year
2026: 9 · 2025: 5
FWCI
8.10
Type
journal article
Language
en
Open access
Licence
Locations
  • The ISME Journal (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (submittedVersion, cc-by-nc-nd)
Funders
  • Yale University
  • National Institutes of Health (5t90de026110-08, 1s10od034405-01, 1s10od023603-01a1)
  • National Institute of Allergy and Infectious Diseases (R01AI152421, R01AI087946)
  • National Institute of Dental and Craniofacial Research (T90 DE026110-07, T90-DE026110, R01DE023810, R01DE031274)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Structural Characterization
  • Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Keywords
Saccharibacteria, Patescibacteria, Candidate Phyla Radiation, type IV pili, twitching motility, host competition, bacterial competition, mock microbial community, priority effects, bacterial symbiosis

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