The evolution of the type VI secretion system as a disintegration weapon

• Published in: PLoS biology Vol. 18; no. 5; p. e3000720
• Main Authors: Smith, William P J, Vettiger, Andrea, Winter, Julius, Ryser, Till, Comstock, Laurie E, Basler, Marek, Foster, Kevin R
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 26-05-2020; Public Library of Science (PLoS)
• Subjects: Analysis; Bacteria; Biochemistry; Biology and Life Sciences; Competition; Computer and Information Sciences; Cost benefit analysis; Disintegration; E coli; Engineering and Technology; Evolution; Firings; Forecasts and trends; Funding; Medicine and Health Sciences; Molecular machines; Physical Sciences; Probiotics; Research and Analysis Methods; Secretion; Simulation; Smith, Andrea; Species; Supervision; Toxins; Weapons; Zoology; United Kingdom; United Kingdom > UK; Switzerland
• ISSN: 1545-7885; 1544-9173; 1545-7885
• DOI: 10.1371/journal.pbio.3000720

The type VI secretion system (T6SS) is a nanomachine used by many bacteria to drive a toxin-laden needle into other bacterial cells. Although the potential to influence bacterial competition is clear, the fitness impacts of wielding a T6SS are not well understood. Here we present a new agent-based model that enables detailed study of the evolutionary costs and benefits of T6SS weaponry during competition with other bacteria. Our model identifies a key problem with the T6SS. Because of its short range, T6SS activity becomes self-limiting, as dead cells accumulate in its way, forming "corpse barriers" that block further attacks. However, further exploration with the model presented a solution to this problem: if injected toxins can quickly lyse target cells in addition to killing them, the T6SS becomes a more effective weapon. We tested this prediction with single-cell analysis of combat between T6SS-wielding Acinetobacter baylyi and T6SS-sensitive Escherichia coli. As predicted, delivery of lytic toxins is highly effective, whereas nonlytic toxins leave large patches of E. coli alive. We then analyzed hundreds of bacterial species using published genomic data, which suggest that the great majority of T6SS-wielding species do indeed use lytic toxins, indicative of a general principle underlying weapon evolution. Our work suggests that, in the T6SS, bacteria have evolved a disintegration weapon whose effectiveness often rests upon the ability to break up competitors. Understanding the evolutionary function of bacterial weapons can help in the design of probiotics that can both establish well and eliminate problem species.