TY - JOUR
T1 - Colonization, competition, and dispersal of pathogens in fluid flow networks
AU - Siryaporn, Albert
AU - Kim, Minyoung Kevin
AU - Shen, Yi
AU - Stone, Howard A.
AU - Gitai, Zemer
N1 - Funding Information:
We thank A. Binns and N. Ouzounov for tobacco plants and J. Gleghorn for an image of chicken embryo vasculature. This work was supported by the NIH Director’s New Innovator Award (1DP2OD004389) to Z.G., a National Science Foundation grant (1330288) to Z.G. and H.A.S., an NIH NRSA postdoctoral fellowship (F32AI095002) to A.S., and a graduate fellowship from the STX Scholarship Foundation to M.K.K.
Publisher Copyright:
© 2015 Elsevier Ltd All rights reserved.
PY - 2015/5/4
Y1 - 2015/5/4
N2 - The colonization of bacteria in complex fluid flow networks, such as those found in host vasculature, remains poorly understood. Recently, it was reported that many bacteria, including Bacillus subtilis [1], Escherichia coli [2], and Pseudomonas aeruginosa [3, 4], can move in the opposite direction of fluid flow. Upstream movement results from the interplay between fluid shear stress and bacterial motility structures, and such rheotactic-like behavior is predicted to occur for a wide range of conditions [1]. Given the potential ubiquity of upstream movement, its impact on population-level behaviors within hosts could be significant. Here, we find that P. aeruginosa communities use a diverse set of motility strategies, including a novel surface-motility mechanism characterized by counter-advection and transverse diffusion, to rapidly disperse throughout vasculature-like flow networks. These motility modalities give P. aeruginosa a selective growth advantage, enabling it to self-segregate from other human pathogens such as Proteus mirabilis and Staphylococcus aureus that outcompete P. aeruginosa in well-mixed non-flow environments. We develop a quantitative model of bacterial colonization in flow networks, confirm our model in vivo in plant vasculature, and validate a key prediction that colonization and dispersal can be inhibited by modifying surface chemistry. Our results show that the interaction between flow mechanics and motility structures shapes the formation of mixed-species communities and suggest a general mechanism by which bacteria could colonize hosts. Furthermore, our results suggest novel strategies for tuning the composition of multi-species bacterial communities in hosts, preventing inappropriate colonization in medical devices, and combatting bacterial infections.
AB - The colonization of bacteria in complex fluid flow networks, such as those found in host vasculature, remains poorly understood. Recently, it was reported that many bacteria, including Bacillus subtilis [1], Escherichia coli [2], and Pseudomonas aeruginosa [3, 4], can move in the opposite direction of fluid flow. Upstream movement results from the interplay between fluid shear stress and bacterial motility structures, and such rheotactic-like behavior is predicted to occur for a wide range of conditions [1]. Given the potential ubiquity of upstream movement, its impact on population-level behaviors within hosts could be significant. Here, we find that P. aeruginosa communities use a diverse set of motility strategies, including a novel surface-motility mechanism characterized by counter-advection and transverse diffusion, to rapidly disperse throughout vasculature-like flow networks. These motility modalities give P. aeruginosa a selective growth advantage, enabling it to self-segregate from other human pathogens such as Proteus mirabilis and Staphylococcus aureus that outcompete P. aeruginosa in well-mixed non-flow environments. We develop a quantitative model of bacterial colonization in flow networks, confirm our model in vivo in plant vasculature, and validate a key prediction that colonization and dispersal can be inhibited by modifying surface chemistry. Our results show that the interaction between flow mechanics and motility structures shapes the formation of mixed-species communities and suggest a general mechanism by which bacteria could colonize hosts. Furthermore, our results suggest novel strategies for tuning the composition of multi-species bacterial communities in hosts, preventing inappropriate colonization in medical devices, and combatting bacterial infections.
UR - http://www.scopus.com/inward/record.url?scp=84929031275&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=84929031275&partnerID=8YFLogxK
U2 - 10.1016/j.cub.2015.02.074
DO - 10.1016/j.cub.2015.02.074
M3 - Article
C2 - 25843031
AN - SCOPUS:84929031275
SN - 0960-9822
VL - 25
SP - 1201
EP - 1207
JO - Current Biology
JF - Current Biology
IS - 9
ER -