TY - JOUR T1 - Tunneling through Time: Horizontal Gene Transfer Constrains the Timing of Methanogen Evolution JF - bioRxiv DO - 10.1101/129494 SP - 129494 AU - Joanna M. Wolfe AU - Gregory P. Fournier Y1 - 2017/01/01 UR - http://biorxiv.org/content/early/2017/04/24/129494.abstract N2 - Archaeal methane production is a major component of the modern carbon cycle. It has been proposed that the metabolism of methanogenic Archaea also contributed to a “methane greenhouse” during the early Archaean Eon, a hypothesis requiring evidence for the evolution of methanogenesis at or before this time. Molecular clock models are frequently used to estimate divergence times of organismal lineages in phylogenies, as well as the order of character acquisition. However, estimating the timing of microbial evolutionary events, especially ones as ancient as the Archaean, is challenged by the lack of diagnostic fossils. Other methods are thus required to calibrate the ages of these clades. Horizontal gene transfers (HGTs) are ubiquitous evolutionary events throughout the Tree of Life, complicating phylogenomic inference by introducing topological conflicts between different gene families across taxa. As HGTs also convey relative timing information between lineages, they can be harnessed to provide geological age constraints for clades lacking a fossil record. We derive a valuable temporal constraint on the timing of the evolution of methanogenesis from a single HGT event from within archaeal methanogen lineages to the ancestor of Cyanobacteria, one of the few microbial clades with recognized crown group fossils. Results of molecular clock analyses using this HGT predict methanogens most likely diverging within Euryarchaeota no later than 3.51 Ga, and methanogenesis itself likely evolving substantially earlier. This timing provides independent support for scenarios wherein microbial methane production has a substantial role in maintaining temperatures on the early Earth.SIGNIFICANCE Methanogenic Archaea are the only organisms known to provide biogeochemically relevant sources of methane on Earth today. While this metabolism is undoubtedly ancient, the oldest geochemical evidence is too young to constrain the emergence of microbial methane, and there is a paucity of reliable microbial fossils to suggest the presence of methanogenic lineages. Molecular clock analyses of methanogenic Archaea, with age constraints derived from an HGT from within methanogens to the ancestor of Cyanobacteria, provide independent support for the hypothesis of an Eoarchaean biogenic methane greenhouse. This approach has broad implications for estimating the ages of microbial clades across the entire Tree of Life, a critical yet largely unexplored frontier of natural history. ER -