History of the Hadean “Living Microfossil” OD1 and Ultra-reducing Environments

Abstract

Phylogenetic analysis is one of the useful tools available for revealing the evolution of life on the Earth; however, it has difficulty in principle distinguishing old and new genomes just by comparing phylogenomic trees. To overcome this difficulty, a new method is introduced which utilizes the Earth's history derived from geologic information to trace genomic evolution. This idea is inspired by Darwin's natural selection, and explains how living organisms change with the environment. In other words, life's genome does not change if the environment remains the same. A key is the birthplace of life on Hadean Earth, which is thought to be an ultra-reducing environment with H 2 produced in abundance through serpentinization. OD1 is a potential microbe that has survived on the Earth since the Hadean. Its habitat, Hakuba-Happo in Japan, is a unique serpentinite-hosted hydrothermal system on land, and it has avoided evolution by remaining in a super-reducing environment from the Hadean to the present. OD1 is regarded as a "living fossil" of the Hadean microbe. Ultra-reducing environments have disappeared over the Earth's history. How has OD1 survived since the Hadean to the present? A possible scenario is proposed based on Plate Tectonics. OD1 habitats have gone through the following transitions:(1) super-reducing environment in a natural nuclear geyser on a primordial continent in the Hadean;(2) serpentinite-hosted hydrothermal system along a mid-oceanic ridge transform fault during the Archean-Proterozoic; (3) subduction-accretion and escape from oxygenated Phanerozoic ocean floor; and, (4) jacked up by growth of accretionary complexes and taking refuge in a hydrothermal system above a volcanic front. OD1 habitats have been reduced with geological age as free oxygen has increased in the surface environment. OD1 may be a "living microfossil" of the Hadean, making its way continuously through ultra-reducing environments on a tightrope.

Size Matters: Ultra-small and Filterable Microorganisms in the Environment

“…Importantly, measurements of replication rates (Brown et al, 2016;Suzuki et al, 2017b) and cryotransmission electron microscopy images showing a dividing cell (Luef et al, 2015) indicated that the extremely small cells of CPR/Patescibacteria are metabolically active and not simply ultramicrocells during starvation. Moreover, CPR/Patescibacteria genomes have been recovered from other environments, such as highly alkaline groundwater (Suzuki et al, 2017b;Sato et al, 2019), lakes (Vigneron et al, 2019), soil (Starr et al, 2018), and marine sediment (Orsi et al, 2018) as well as the human microbiome (He et al, 2015) and dolphin mouse (Dudek et al, 2017), suggesting a wide distribution across environments. Besides describing ultra-small life forms with high phylogenetic novelty, genomic analyses of CPR/Patescibacteria members have provided information on their small genomes, fermentative metabolism, and other unusual features (e.g., selfsplicing introns varying in length and proteins encoded within their 16S rRNA genes; Brown et al, 2015;Castelle et al, 2018).…”

Single-Cell Genomics of Novel Actinobacteria With the Wood–Ljungdahl Pathway Discovered in a Serpentinizing System

“…The microbial communities of the Hakuba Happo hot spring (36 • 42 N, 137 • 48 E) ophiolite located along the Itoigawa-Shizuoka Tectonic Line in central Honshu, Japan have yet to be investigated. This region consists of an ultramafic rock body that is ∼580 Ma old (Sato et al, 2019) and has ongoing serpentinization activity (Suda et al, 2014(Suda et al, , 2017. The geochemistry of the site is characteristic of a serpentinite-hosted system, with highly alkaline waters (pH > 10.6) and high concentrations of dissolved H 2 (201-664 µM) and CH 4 (124-201 µM) (Suda et al, 2014).…”

Overview of the Special Issue “The Hadean World (Part II): Preparing a Site for the First Life“

“…Based on these observational facts, Hakuba OD1 is expected to contribute significantly to origin-of-life research. Sato et al (2019) discuss the history of the habitat of Hakuba OD1 since the Hadean. Atmospheric free oxygen increased with time, and the hydrogen environment of the Earth decreased.…”

“…If Hakuba OD1 moves along the mid-oceanic ridge, it can survive in a hydrogen-rich environment. Subsequently, the mid-oceanic ridge must be taken into an orogenic belt, such as that at Hakuba, which is discussed by Sato et al (2019) . In addition, such a tectonic setting had to have been made by 600 Ma when atmospheric free oxygen reached the present level.…”