Tracing the evolution of tail fibers and their receptors in historical metagenomes

Hernán Burbano

Hernán Burbano

University College London

Centre for Life's Origins and Evolution/Department of Genetics, Evolution and Environment

Hernán studied veterinary medicine and biology (1996-2006) at the Universidad Nacional de Colombia in Bogotá. He then moved to the Max Planck Institute (MPI) for Evolutionary Anthropology in Leipzig, Germany, where he worked on ancient genomics of humans and archaic hominins under the supervision of Svante Pääbo and Michael Lachmann. Hernán obtained a PhD in evolutionary genetics from the University of Leipzig in 2012. Hernán then relocated as a postdoctoral researcher (2012-2014) at the MPI for Developmental Biology in Tuebingen, Germany, under the supervision of Detlef Weigel. There, he integrated plant evolutionary genomics and ancient DNA. From 2014 to 2019, Hernán led the Research Group for Ancient Genomics and Evolution at the MPI for Developmental Biology, before joining the UCL Centre for Life’s Origins and Evolution as an Associate Professor in 2019. Hernán was promoted to Full Professor of Ancient Genomics and Evolution in 2024. In 2019, Hernán was awarded a Royal Society Wolfson Fellowship, a scheme jointly funded by the Royal Society and the Wolfson Foundation that enables the recruitment of outstanding research leaders to the UK from overseas. In 2020, Hernán was honoured with a Philip Leverhulme Prize for outstanding contributions to Biological Sciences.

Authors: Cui J1, Latorre SM1, Backman T2, Karasov T2, Burbano HA2

Affiliations: (1). Centre for Life’s Origins and Evolution, Department of Genetics, Evolution and Environment, University College London, London (UK) (2). School of Biological Sciences, University of Utah, Salt Lake City, UT 84112 (USA)

Tail fibers of bacteriophages and phage tail-like elements such as R-type tailocins evolve rapidly, giving rise to extensive genetic diversity within phage and bacterial populations. This diversity is reflected in the co-existence of highly divergent tail fiber variants segregating at different frequencies. In wild populations of Pseudomonas viridiflava associated with Arabidopsis thaliana, we previously identified such divergent tailocin variants, highlighting the dynamic nature of these molecular weapons. However, the evolutionary timescale over which tail fiber turnover occurs—and by extension, the durability of bacterial sensitivity or resistance to specific tailocin variants—remains poorly understood. To investigate this, we combined the analysis of present-day P. viridiflava genomes with metagenomic data derived from historical A. thaliana herbarium specimens spanning the last 200 years. By applying ancient DNA extraction and analysis techniques, we reconstructed tailocin gene clusters and identified the tail fiber haplotypes that have segregated across centuries. Additionally, we examined the presence and absence of genes involved in the biosynthesis of tailocin receptors, focusing on components of the bacterial outer membrane, particularly the O-antigen. Our findings reveal long-term maintenance of tail fiber diversity and suggest a co-evolutionary dynamic between specific tail fiber variants and genes involved in receptor biosynthesis. This study demonstrates how historical metagenomes offer a powerful lens through which to explore microbial genetic diversity across time, uncovering the evolutionary pressures that shape tail fiber interactions in natural populations.