Metagenome-assembled genome of the glacier alga Ancylonema yields insights into the evolution of streptophyte life on ice and land.

Contemporary glaciers are inhabited by streptophyte algae that balance photosynthesis and growth with tolerance of low temperature, desiccation and UV radiation. These same environmental challenges have been hypothesised as the driving force behind the evolution of land plants from streptophyte algal ancestors in the Cryogenian (720-635 million years ago). We sequenced, assembled and analysed the metagenome-assembled genome of the glacier alga Ancylonema nordenskiöldii to investigate its adaptations to life in ice, and whether this represents a vestige of Cryogenian exaptations. Phylogenetic analysis confirms the placement of glacier algae within the sister lineage to land plants, Zygnematophyceae. The metagenome-assembled genome is characterised by an expansion of genes involved in tolerance of high irradiance and UV light, while lineage-specific diversification is linked to the novel screening pigmentation of glacier algae. We found no support for the hypothesis of a common genomic basis for adaptations to ice and to land in streptophytes. Comparative genomics revealed that the reductive morphological evolution in the ancestor of Zygnematophyceae was accompanied by reductive genome evolution. This first genome-scale data for glacier algae suggests an Ancylonema-specific adaptation to the cryosphere, and sheds light on the genome evolution of land plants and Zygnematophyceae.

Alpine glacier algal bloom during a record melt year.

Glacier algal blooms dominate the surfaces of glaciers and ice sheets during summer melt seasons, with larger blooms anticipated in years that experience the greatest melt. Here, we characterize the glacier algal bloom proliferating on Morteratsch glacier, Switzerland, during the record 2022 melt season, when the Swiss Alps lost three times more ice than the decadal average. Glacier algal cellular abundance (cells ml-1), biovolume (µm3 cell-1), photophysiology (Fv/Fm, rETRmax), and stoichiometry (C:N ratios) were constrained across three elevations on Morteratsch glacier during late August 2022 and compared with measurements of aqueous geochemistry and outputs of nutrient spiking experiments. While a substantial glacier algal bloom was apparent during summer 2022, abundances ranged from 1.78 × 104 to 8.95 × 105 cells ml-1 of meltwater and did not scale linearly with the magnitude of the 2022 melt season. Instead, spatiotemporal heterogeneity in algal distribution across Morteratsch glacier leads us to propose melt-water-redistribution of (larger) glacier algal cells down-glacier and presumptive export of cells from the system as an important mechanism to set overall bloom carrying capacity on steep valley glaciers during high melt years. Despite the paradox of abundant glacier algae within seemingly oligotrophic surface ice, we found no evidence for inorganic nutrient limitation as an important bottom-up control within our study site, supporting our hypothesis above. Fundamental physical constraints may thus cap bloom carrying-capacities on valley glaciers as 21st century melting continues.

Cryogenian Origins of Multicellularity in Archaeplastida.

Earth was impacted by global glaciations during the Cryogenian (720 to 635 million years ago; Ma), events invoked to explain both the origins of multicellularity in Archaeplastida and radiation of the first land plants. However, the temporal relationship between these environmental and biological events is poorly established, due to a paucity of molecular and fossil data, precluding resolution of the phylogeny and timescale of archaeplastid evolution. We infer a time-calibrated phylogeny of early archaeplastid evolution based on a revised molecular dataset and reappraisal of the fossil record. Phylogenetic topology testing resolves deep archaeplastid relationships, identifying two clades of Viridiplantae and placing Bryopsidales as sister to the Chlorophyceae. Our molecular clock analysis infers an origin of Archaeplastida in the late-Paleoproterozoic to early-Mesoproterozoic (1712 to 1387 Ma). Ancestral state reconstruction of cytomorphological traits on this time-calibrated tree reveals many of the independent origins of multicellularity span the Cryogenian, consistent with the Cryogenian multicellularity hypothesis. Multicellular rhodophytes emerged 902 to 655 Ma while crown-Anydrophyta (Zygnematophyceae and Embryophyta) originated 796 to 671 Ma, broadly compatible with the Cryogenian plant terrestrialization hypothesis. Our analyses resolve the timetree of Archaeplastida with age estimates for ancestral multicellular archaeplastids coinciding with the Cryogenian, compatible with hypotheses that propose a role of Snowball Earth in plant evolution.

The origin and early evolution of plants.

Plant (archaeplastid) evolution has transformed the biosphere, but we are only now beginning to learn how this took place through comparative genomics, phylogenetics, and the fossil record. This has illuminated the phylogeny of Archaeplastida, Viridiplantae, and Streptophyta, and has resolved the evolution of key characters, genes, and genomes - revealing that many key innovations evolved long before the clades with which they have been casually associated. Molecular clock analyses estimate that Streptophyta and Viridiplantae emerged in the late Mesoproterozoic to late Neoproterozoic, whereas Archaeplastida emerged in the late-mid Palaeoproterozoic. Together, these insights inform on the coevolution of plants and the Earth system that transformed ecology and global biogeochemical cycles, increased weathering, and precipitated snowball Earth events, during which they would have been key to oxygen production and net primary productivity (NPP).

Water-related innovations in land plants evolved by different patterns of gene cooption and novelty.

The origin of land plants and their descendants was marked by the evolution of key adaptations to life in terrestrial environments such as roots, vascular tissue and stomata. Though these innovations are well characterized, the evolution of the genetic toolkit underlying their development and function is poorly understood. We analysed molecular data from 532 species to investigate the evolutionary origin and diversification of genes involved in the development and regulation of these adaptations. We show that novel genes in the first land plants led to the single origin of stomata, but the stomatal closure of seed plants resulted from later gene expansions. By contrast, the major mechanism leading to the origin of vascular tissue was cooption of genes that emerged in the first land plants, enabling continuous water transport throughout the ancestral vascular plant. In turn, new key genes in the ancestors of plants with true leaves and seed plants led to the emergence of roots and lateral roots. The analysis highlights the different modes of evolution that enabled plants to conquer land, suggesting that gene expansion and cooption are the most common mechanisms of biological innovation in plant evolutionary history.

Evolutionary Origins of Drought Tolerance in Spermatophytes.

It is commonly known that drought stress is a major constraint limiting crop production. Drought stress and associated drought tolerance mechanisms are therefore under intense investigation with the view to future production of drought tolerant crops. With an ever-growing population and variable climate, novel approaches need to be considered to sustainably feed future generations. In this context, definitions of drought tolerance are highly variable, which poses a major challenge for the systematic assessment of this trait across the plant kingdom. Furthermore, drought tolerance is a polygenic trait and understanding the evolution of this complex trait may inform us about patterns of gene gain and loss in relation to diverse drought adaptations. We look at the transition of plants from water to land, and the role of drought tolerance in enabling this transition, before discussing the first drought tolerant plant and common drought responses amongst vascular plants. We reviewed the distribution of a combined "drought tolerance" trait in very broad terms to encompass different experimental systems and definitions used in the current literature and assigned a binary trait "tolerance vs. sensitivity" in 178 extant plant species. By simplifying drought responses of plants into this "binary" trait we were able to explore the evolution of drought tolerance across the wider plant kingdom, compared to previous studies. We show how this binary "drought tolerance/sensitivity" trait has evolved and discuss how incorporating this information into an evolutionary genomics framework could provide insights into the molecular mechanisms underlying extreme drought adaptations.

The Role of Ribosomal Protein S6 Kinases in Plant Homeostasis.

The p70 ribosomal S6 kinase (S6K) family is a group of highly conserved kinases in eukaryotes that regulates cell growth, cell proliferation, and stress response via modulating protein synthesis and ribosomal biogenesis. S6Ks are downstream effectors of the Target of Rapamycin (TOR) pathway, which connects nutrient and energy signaling to growth and homeostasis, under normal and stress conditions. The plant S6K family includes two isoforms, S6K1 and S6K2, which, despite their high level of sequence similarity, have distinct functions and regulation mechanisms. Significant advances on the characterization of human S6Ks have occurred in the past few years, while studies on plant S6Ks are scarce. In this article, we review expression and activation of the two S6K isoforms in plants and we discuss their roles in mediating responses to stresses and developmental cues.

Microbial Diversity of Pinnacle and Conical Microbial Mats in the Perennially Ice-Covered Lake Untersee, East Antarctica.

Antarctic perennially ice-covered lakes provide a stable low-disturbance environment where complex microbially mediated structures can grow. Lake Untersee, an ultra-oligotrophic lake in East Antarctica, has the lake floor covered in benthic microbial mat communities, where laminated organo-sedimentary structures form with three distinct, sympatric morphologies: small, elongated cuspate pinnacles, large complex cones and flat mats. We examined the diversity of prokaryotes and eukaryotes in pinnacles, cones and flat microbial mats using high-throughput sequencing of 16S and 18S rRNA genes and assessed how microbial composition may underpin the formation of these distinct macroscopic mat morphologies under the same environmental conditions. Our analysis identified distinct clustering of microbial communities according to mat morphology. The prokaryotic communities were dominated by Cyanobacteria, Proteobacteria, Verrucomicrobia, Planctomycetes, and Actinobacteria. While filamentous Tychonema cyanobacteria were common in all mat types, Leptolyngbya showed an increased relative abundance in the pinnacle structures only. Our study provides the first report of the eukaryotic community structure of Lake Untersee benthic mats, which was dominated by Ciliophora, Chlorophyta, Fungi, Cercozoa, and Discicristata. The eukaryote richness was lower than for prokaryote assemblages and no distinct clustering was observed between mat morphologies. These findings suggest that cyanobacterial assemblages and potentially other bacteria and eukaryotes may influence structure morphogenesis, allowing distinct structures to form across a small spatial scale.

The Origin of Land Plants Is Rooted in Two Bursts of Genomic Novelty.

Over the last 470 Ma, plant evolution has seen major evolutionary transitions, such as the move from water to land and the origins of vascular tissues, seeds, and flowers [1]. These have resulted in the evolution of terrestrial flora that has shaped modern ecosystems and the diversification of the Plant Kingdom, Viridiplantae, into over 374,000 described species [2]. Each of these transitions was accompanied by the gain and loss of genes in plant genomes. For example, whole-genome duplications are known to be fundamental to the origins of both seed and flowering plants [3, 4]. With the ever-increasing quality and quantity of whole-genome data, evolutionary insight into origins of distinct plant groups using comparative genomic techniques is now feasible. Here, using an evolutionary genomics pipeline to compare 208 complete genomes, we analyze the gene content of the ancestral genomes of the last common ancestor of land plants and all other major groups of plant. This approach reveals an unprecedented level of fundamental genomic novelties in two nodes related to the origin of land plants: the first in the origin of streptophytes during the Ediacaran and another in the ancestor of land plants in the Ordovician. Our findings highlight the biological processes that evolved with the origin of land plants and emphasize the importance of conserved gene novelties in plant diversification. Comparisons to other eukaryotic studies suggest a separation of the genomic origins of multicellularity and terrestrialization in plants.