The genome of Pasteuria ramosa reveals a high turnover rate of collagen-like genes

Abstract

Collagen-like proteins (CLP) are commonly found in many pathogenic bacteria where they serve as adhesins to attach to host tissue. The repetition of the amino-acid pattern (Gly-Xaa-Yaa)n is the major feature of collagen and is essential to the formation of its stable triple helical structure. In the Daphnia magna-Pasteuria ramosa system, a model system for studying antagonistic coevolution, a specific CLP in the virulent parasite P. ramosa plays a pivotal role in host attachment, regulated by matching allele model. Recognizing the crucial role of CLPs in the infection process, we aimed to enhance our understanding of P. ramosa-CLPs by sequencing high-quality genomes of two isolates, using long-read technology. An analysis of a CLP gene tree of representative Bacillota species revealed a clear radiation of these genes in P. ramosa, which was not found in the closely related Pasteuria penetrans. A comparison of the isolates reveals a high synteny, with the exception of a few duplications and inversions, mainly involving CLPs or transposases. Across isolates, we observed a recent burst of transposases as well as duplications of CLP genes. On average, CLP genes are well conserved between isolates, but the presence/absence of individual CLP genes is not fully shared, with 39 and 43 genes in the two isolates. Our findings suggest a rapid radiation of CLP genes combined with a birth and death process of the large P. ramosa-CLP gene family, possibly driven by transposition and coevolution. ImportanceAlthough the host-pathogen Daphnia magna-Pasteuria ramosa system has served as a model for coevolution, we have, to date, lacked high-quality genomic resources for the parasite, as is the case for many such systems. By presenting a complete assembly of two distinct P. ramosa isolates, our study addresses this lack and provides deeper insights into the P. ramosa Collagen Like Protein (CLP) family, essential proteins involved in attachment to the host. We discover that the rapid radiation of CLP genes in P. ramosa appears to be driven by transposition and coevolution, enabling the parasite to adapt to host resistance mechanisms. These insights improve our understanding of host-parasite interactions and pave the way for comparative genomic analyses to better understand the evolution of these genes. They also have broader implications for disease control and therapeutic development targeting pathogenic bacteria adhesion mechanisms.