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Deep-branching Chloroflexota lineages illuminate the eco-evolutionary foundation of cross-ecosystem colonization

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Abstract

Bacteria span Earth’s ecosystems, coupling ecological versatility with genome-architectural reconfiguration across shifting physicochemical conditions. Yet the genomic routes by which free-living lineages cross ecosystem boundaries, and the consequences for genome architecture, remain poorly understood. Here, we use comparative and evolutionary genomics to investigate a soil-to-sediment-to-freshwater transition in Limnocylindria, an abundant clade within the Chloroflexota phylum. Two sister families show contrasting strategies. CSP1-4 expands genomes through niche-specific gene acquisition, whereas Limnocylindraceae undergoes genome reduction and metabolic simplification—revealing alternative evolutionary routes to similar ecological outcomes. In Limnocylindraceae, the loss of key DNA glycosylases coincides with degradation of base excision repair and is consistent with a hypermutator state that may have accelerated genomic erosion during freshwater specialization, potentially facilitating ecological expansion. This reductive genome trajectory is associated with a freshwater-adapted lineage with unexpectedly high GC content, challenging canonical links between base composition and genome size. While mutational processes appear to dominate genome restructuring, proteome-level patterns suggest selection favoring carbon- and nitrogen-efficient amino acid usage, implying that adaptive refinement can emerge alongside primarily non-adaptive dynamics. Overall, our findings are consistent with mutation-driven genome reduction and proteome optimization acting in concert to support cross-ecosystem boundary crossing and freshwater specialization in a free-living Chloroflexota lineage.

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Data availability

All genomic data utilized in this study is publicly available. 236 MAG IDs and their NCBI accession numbers are provided in Supp. Data S1. NCBI SRA IDs are provided for 14,644 metagenomes in Supp. Data S5. All additional important data supporting the study’s conclusions are included in this publication and its Supp. Data 2–15. Source data are provided with this paper.

Code availability

The source code generated in this study is publicly available on GitHub at (https://github.com/MiELevog/Cross-ecosystem-colonization) (https://doi.org/10.5281/zenodo.18416940)91.

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Acknowledgements

We are grateful to Jakob Pernthaler for his thorough and constructive review of the manuscript draft. A.-S.A. and L.S.M. were supported by the Ambizione grant PZ00P3_193240 (Swiss National Science Foundation). C.H. was supported by the research grant 10000877 (Swiss National Science Foundation).

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  1. Limnological Station, Department of Plant and Microbial Biology, University of Zurich, Kilchberg, Switzerland

    Lucas Serra Moncadas, Alisa Shakurova, Cyrill Hofer & Adrian-Stefan Andrei

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  1. Lucas Serra Moncadas
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Conceptualization: A.-S.A. and L.S.M. Bioinformatics: L.S.M., C.H., and A.-S.A. CARD-FISH: A.S. Statistics: L.S.M. Writing, original draft: A.-S.A. with input from L.S.M. Writing, review, and editing: L.S.M., A.S., and C.H. Funding acquisition: A.-S.A.

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Serra Moncadas, L., Shakurova, A., Hofer, C. et al. Deep-branching Chloroflexota lineages illuminate the eco-evolutionary foundation of cross-ecosystem colonization.
Nat Commun (2026). https://doi.org/10.1038/s41467-026-71228-y

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