Distinct core minor pilin complexes prime specialized type IV filaments in cyanobacteria
5 affiliations
- 1Molecular Genetics of Prokaryotes, Faculty of Biology, University of Freiburg, Freiburg, Germany
- 2Department of Agricultural Chemistry, Tokyo University of Agriculture, Tokyo, Japan
- 3Molecular Biology of Archaea, Faculty of Biology, University of Freiburg, Freiburg, Germany
- 4CIBSS-Centre for Integrative Biological Signalling Studies, University of Freiburg, Freiburg, Germany
- 5Biochemistry and Functional Proteomics, Faculty of Biology, University of Freiburg, Freiburg, Germany
Abstract
The model cyanobacterium, Synechocystis sp. PCC 6803 encodes in addition to the major pilin of the Type IV pilus filament, an extensive, partially uncharacterized repertoire of minor pilins. For those cyanobacterial minor pilins that have been characterized, their roles span a surprisingly diverse range of functions. To elucidate the roles of uncharacterized minor pilins in a systematic way, we applied structural phylogenomics across 90 genomes, classifying cyanobacterial pilins into six conserved families that form two distinct putative core priming complexes. We demonstrate that these complexes initiate the assembly of two morphologically distinct Type IV pilus filaments: short, hyper-dynamic pili for natural competence, and long, adhesive pili for motility and phototaxis. Structural analysis revealed a conserved beta-solenoid domain in PilX subunits, which we propose fulfills the capping function of PilY1 homologs. Proteomic data indicate that the minor pilin PilX2 facilitates the assembly of motility pili, which is required to maintain DnaJ3 co-chaperone levels and trigger cAMP-dependent surface sensing. These findings challenge the concept of a single multipurpose pilus, establishing that cyanobacteria utilize a shared machinery to assemble two specialized filaments, each primed by distinct core minor pilin complexes to meet the conflicting biophysical requirements of DNA uptake and surface motility. Author summary: Many bacteria use microscopic, hair-like filaments called Type IV pili to crawl across surfaces or take up DNA from their surroundings. In our study, we investigated how cyanobacteria, photosynthetic microbes ubiquitous in oceans, lakes, and wetlands, manage these different tasks. Because the proteins that form these filaments have changed significantly over billions of years, it is difficult to compare them using traditional methods. We instead used a computational approach to compare their three-dimensional shapes. We discovered that cyanobacteria assemble two distinct types of filaments using the same basic machinery. By swapping out a specific set of “starter” proteins at the tip, the cell can produce either short, dynamic filaments for DNA capture or long fibers specialized for surface attachment that act as grappling hooks to pull the cell toward light. Our findings reveal an elegant evolutionary strategy: instead of building two entirely separate nanomachines, these microbes use a single, versatile motor to drive specialized tools. This allows them to meet conflicting physical requirements, such as the need for a quick reach versus a steady, strong grip, simply by switching a small set of starter proteins.
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BibTeX
@article{schuergers2026distinct,
title = {{Distinct core minor pilin complexes prime specialized type IV filaments in cyanobacteria}},
author = {Nils Schuergers and Lars Wittig and Gen Enomoto and Julia Herz and Shamphavi Sivabalasarma and Katharina Ruoff and Friedel Drepper and Sonja-Verena Albers and Pitter F. Huesgen and Annegret Wilde},
journal = {PLOS Genetics},
year = {2026},
month = oct,
doi = {10.1371/journal.pgen.1012337},
url = {https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1012337},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Distinct core minor pilin complexes prime specialized type IV filaments in cyanobacteria
AU - Nils Schuergers
AU - Lars Wittig
AU - Gen Enomoto
AU - Julia Herz
AU - Shamphavi Sivabalasarma
AU - Katharina Ruoff
AU - Friedel Drepper
AU - Sonja-Verena Albers
AU - Pitter F. Huesgen
AU - Annegret Wilde
PY - 2026
DA - 2026/10/26
JO - PLOS Genetics
DO - 10.1371/journal.pgen.1012337
UR - https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1012337
AB - The model cyanobacterium, Synechocystis sp. PCC 6803 encodes in addition to the major pilin of the Type IV pilus filament, an extensive, partially uncharacterized repertoire of minor pilins. For those cyanobacterial minor pilins that have been characterized, their roles span a surprisingly diverse range of functions. To elucidate the roles of uncharacterized minor pilins in a systematic way, we applied structural phylogenomics across 90 genomes, classifying cyanobacterial pilins into six conserved families that form two distinct putative core priming complexes. We demonstrate that these complexes initiate the assembly of two morphologically distinct Type IV pilus filaments: short, hyper-dynamic pili for natural competence, and long, adhesive pili for motility and phototaxis. Structural analysis revealed a conserved beta-solenoid domain in PilX subunits, which we propose fulfills the capping function of PilY1 homologs. Proteomic data indicate that the minor pilin PilX2 facilitates the assembly of motility pili, which is required to maintain DnaJ3 co-chaperone levels and trigger cAMP-dependent surface sensing. These findings challenge the concept of a single multipurpose pilus, establishing that cyanobacteria utilize a shared machinery to assemble two specialized filaments, each primed by distinct core minor pilin complexes to meet the conflicting biophysical requirements of DNA uptake and surface motility. Author summary: Many bacteria use microscopic, hair-like filaments called Type IV pili to crawl across surfaces or take up DNA from their surroundings. In our study, we investigated how cyanobacteria, photosynthetic microbes ubiquitous in oceans, lakes, and wetlands, manage these different tasks. Because the proteins that form these filaments have changed significantly over billions of years, it is difficult to compare them using traditional methods. We instead used a computational approach to compare their three-dimensional shapes. We discovered that cyanobacteria assemble two distinct types of filaments using the same basic machinery. By swapping out a specific set of “starter” proteins at the tip, the cell can produce either short, dynamic filaments for DNA capture or long fibers specialized for surface attachment that act as grappling hooks to pull the cell toward light. Our findings reveal an elegant evolutionary strategy: instead of building two entirely separate nanomachines, these microbes use a single, versatile motor to drive specialized tools. This allows them to meet conflicting physical requirements, such as the need for a quick reach versus a steady, strong grip, simply by switching a small set of starter proteins.
SN - 1553-7404
ER -