Evolutionary selection of biofilm-mediated extended phenotypes in Yersinia pestis in response to a fluctuating environment

Yu‐Jun Cui ,Qingwen Zhang,Bing Xu,Changhong Guo ,Qi Zhang ,Xianwei Yang,Zongmin Du,Boris V Schmid,Chao Yang,Jing Yang,Haihong Fang,Wanbing Liu,Xuanming Ding ,Yújiāng Zhāng ,Nils Chr Stenseth,Min Wang,Shanqian Huang,Yajun Song,W Ryan Easterday,Kjetill S Jakobsen,Huaiyu Tian,Hanli Cao,Yarong Wu,Ruifu Yang

doi:10.1038/s41467-019-14099-w

Abstract

Yersinia pestis is transmitted from fleas to rodents when the bacterium develops an extensive biofilm in the foregut of a flea, starving it into a feeding frenzy, or, alternatively, during a brief period directly after feeding on a bacteremic host. These two transmission modes are in a trade-off regulated by the amount of biofilm produced by the bacterium. Here by investigating 446 global isolated Y. pestis genomes, including 78 newly sequenced isolates sampled over 40 years from a plague focus in China, we provide evidence for strong selection pressures on the RNA polymerase ω-subunit encoding gene rpoZ. We demonstrate that rpoZ variants have an increased rate of biofilm production in vitro, and that they evolve in the ecosystem during colder and drier periods. Our results support the notion that the bacterium is constantly adapting—through extended phenotype changes in the fleas—in response to climate-driven changes in the niche.

Highlights

Yersinia pestis is transmitted from fleas to rodents when the bacterium develops an extensive biofilm in the foregut of a flea, starving it into a feeding frenzy, or, alternatively, during a brief period directly after feeding on a bacteremic host
Increased levels of biofilm formation lead to a better ability of the bacterium to maintain itself in the foregut of the flea[6], and improve its chances to persist in the flea gut for long enough to successfully transmit through blockage-induced transmission
To study whether evolutionary trade-offs like the one above occur in Y. pestis in a natural setting, we investigated the temporal dynamics of Y. pestis within a wildlife plague reservoir of ground squirrels (Spermophilus undulatus) and their fleas (Citellophilus tesquorum)

Summary

Introduction

Yersinia pestis is transmitted from fleas to rodents when the bacterium develops an extensive biofilm in the foregut of a flea, starving it into a feeding frenzy, or, alternatively, during a brief period directly after feeding on a bacteremic host. Increased levels of biofilm formation lead to a better ability of the bacterium to maintain itself in the foregut of the flea[6], and improve its chances to persist in the flea gut for long enough to successfully transmit through blockage-induced transmission. These increased levels of biofilm formation decreases the efficiency of early-phase transmission[4]. According to the extended phenotype perspective, the genotype of the bacterium influences the phenotype and/or the behavior of the host (flea) species through the type of biofilm formation affecting the flea’s “feeding” behavior)

Methods

Results

Conclusion