Isolation of a Novel Thermophilic Methanogen and the Evolutionary History of the Class Methanobacteria

SIMPLE SUMMARY: The methanogenesis pathway via methanogens dates back to the Hadean or Archaean Earth. These methanogens are considered to have a thermophilic origin and are presently ubiquitously distributed across anaerobic environments. The class Methanobacteria comprises methanogens that are found extensively in geothermal environments, such as hot springs and hydrothermal vents, and their evolutionary history and how they adapted to different temperatures remain unclear. In this study, we isolated a novel species of the class Methanobacteria from a natural hot spring in Tengchong, China. This species can produce methane, utilizing hydrogen and carbon dioxide, at 65 °C. In addition, we found that members of the class Methanobacteria originated in a geothermal niche and then evolved to adapt to ambient temperatures; during this process, thermal adaptation genes were lost and a wide range of metabolic genes were acquired. This research on methanogen evolution will help us understand how life originated in geothermal environments and then spread extensively across present-day Earth. ABSTRACT: Methanogens can produce methane in anaerobic environments via the methanogenesis pathway, and are regarded as one of the most ancient life forms on Earth. They are ubiquitously distributed across distinct ecosystems and are considered to have a thermophilic origin. In this study, we isolated, pure cultured, and completely sequenced a single methanogen strain DL9LZB001, from a hot spring at Tengchong in Southwest China. DL9LZB001 is a thermophilic and hydrogenotrophic methanogen with an optimum growth temperature of 65 °C. It is a putative novel species, which has been named Methanothermobacter tengchongensis—a Class I methanogen belonging to the class Methanobacteria. Comparative genomic and ancestral analyses indicate that the class Methanobacteria originated in a hyperthermal environment and then evolved to adapt to ambient temperatures. This study extends the understanding of methanogens living in geothermal niches, as well as the origin and evolutionary history of these organisms in ecosystems with different temperatures.