Early Terrestrialization: Transition from Algal to Bryophyte Grade

Abstract

Terrestrialization of planet Earth likely began more than a billion years ago with the colonization of land by bacteria, followed by eukaryotic algae much like those occupying modern soils and shallow freshwaters and the earliest embryophytes, close relatives of modern bryophytes. Colonization of land by algae and the first plants was prerequisite to the development of organic-rich soils that later supported more complex plant communities dominated by vascular plants, and the rise of land animals. Consequently, understanding terrestrialization sheds light on Earth’s early biological carbon cycling processes, which aids our understanding of global biogeochemistry in particular, and planetary science in general. Comprehending the process and pattern of ancient terrestrialization requires both neontological and paleontological approaches. Molecular phylogenetics provides the necessary scaffold upon which terrestrialization processes can be analyzed by comparing the structures, physiologies, microbiomes, and genomes of earliest-branching lineages of modern liverworts and mosses to those of plants’ closest modern green algal relatives, the streptophyte algae (also known as charophyte algae or charophycean green algae). Such studies reveal that modern bryophytes inherited spore and body desiccation-resistance, degradation-resistant lignin-like phenolic cell wall polymers, and other physiological traits useful in terrestrial habitats from ancestral algae, indicating that such features were also traits of the earliest land plants. Because modern algae and bryophytes possess degradation-resistant cells or tissues, artificially degrading them for comparison with enigmatic microscopic fossils has been a fruitful way to identify remains of early terrestrial photosynthesizers and thus illuminate terrestrialization patterns. Microfossils cited as evidence for terrestrial cyanobacteria occur beginning more than 1,000 million years ago in the Precambrian, as do probable remains of freshwater and terrestrial eukaryotic algae. Some microfossils obtained from 499 to 511 million year old deposits closely resemble the modern complex streptophyte alga Coleochaete when it has been cultivated subaerially, suggesting that streptophytes were able to photosynthesize on land by the Middle Cambrian. Other microfossils observed in Cambrian and early Middle Ordovician deposits may also be remains of land plants. Remains of early liverwort-like land plants are confidently known from 470 million year old mid-Ordovician deposits, as are possible fossils of early-divergent mosses. Microfossils and macrofossils that have been compared to modern liverwort and moss taxa occur in Silurian to Devonian deposits laid down before and during the first major diversification of the vascular plants in the Late Silurian to Early Devonian, 407–418 million years ago. Such evidence, together with molecular phylogenies and clock analyses, demonstrates that bryophytes and streptophyte algal relatives were the dominant eukaryotic photosynthesizers on land from about 500–400 million years ago, prior to and during the earliest stages of vascular plant evolution. Because bryophytes and streptophyte algae produce degradation-resistant carbon that can be sequestered, thereby reducing atmospheric carbon dioxide levels, models suggest that they had significant impacts on Earth’s carbon cycle for at least 40 million years and perhaps more than 100 million years. We can thus predict that other Earth-like, habitable-zone planets may likewise experience long periods during which organisms equivalent to earthly terrestrial streptophyte algae and bryophytes impact planetary biogeochemistry.