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.

Adaptation versus plastic responses to temperature, light, and nitrate availability in cultured snow algal strains.

Snow algal blooms are widespread, dominating low temperature, high light, and oligotrophic melting snowpacks. Here, we assessed the photophysiological and cellular stoichiometric responses of snow algal genera Chloromonas spp. and Microglena spp. in their vegetative life stage isolated from the Arctic and Antarctic to gradients in temperature (5 - 15°C), nitrate availability (1 - 10 µmol L-1), and light (50 and 500 µmol photons m-2 s-1). When grown under gradients in temperature, measured snow algal strains displayed Fv/Fm values increased by ∼115% and electron transport rates decreased by ∼50% at 5°C compared to 10 and 15°C, demonstrating how low temperatures can mimic high light impacts to photophysiology. When using carrying capacity as opposed to growth rate as a metric for determining the temperature optima, these snow algal strains can be defined as psychrophilic, with carrying capacities ∼90% higher at 5°C than warmer temperatures. All strains approached Redfield C:N stoichiometry when cultured under nutrient replete conditions regardless of temperature (5.7 ± 0.4 across all strains), whereas significant increases in C:N were apparent when strains were cultured under nitrate concentrations that reflected in situ conditions (17.8 ± 5.9). Intra-specific responses in photophysiology were apparent under high light with Chloromonas spp. more capable of acclimating to higher light intensities. These findings suggest that in situ conditions are not optimal for the studied snow algal strains, but they are able to dynamically adjust both their photochemistry and stoichiometry to acclimate to these conditions.

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).

Macro-Nutrient Stoichiometry of Glacier Algae From the Southwestern Margin of the Greenland Ice Sheet.

Glacier algae residing within the surface ice of glaciers and ice sheets play globally significant roles in biogeochemical cycling, albedo feedbacks, and melt of the world's cryosphere. Here, we present an assessment of the macro-nutrient stoichiometry of glacier algal assemblages from the southwestern Greenland Ice Sheet (GrIS) margin, where widespread glacier algal blooms proliferate during summer melt seasons. Samples taken during the mid-2019 ablation season revealed overall lower cellular carbon (C), nitrogen (N), and phosphorus (P) content than predicted by standard microalgal cellular content:biovolume relationships, and elevated C:N and C:P ratios in all cases, with an overall estimated C:N:P of 1,997:73:1. We interpret lower cellular macro-nutrient content and elevated C:N and C:P ratios to reflect adaptation of glacier algal assemblages to their characteristic oligotrophic surface ice environment. Such lower macro-nutrient requirements would aid the proliferation of blooms across the nutrient poor cryosphere in a warming world. Up-scaling of our observations indicated the potential for glacier algal assemblages to accumulate ∼ 29 kg C km2 and ∼ 1.2 kg N km2 within our marginal surface ice location by the mid-ablation period (early August), confirming previous modeling estimates. While the long-term fate of glacier algal autochthonous production within surface ice remains unconstrained, data presented here provide insight into the possible quality of dissolved organic matter that may be released by assemblages into the surface ice environment.

Over Winter Microbial Processes in a Svalbard Snow Pack: An Experimental Approach.

Snow packs cover large expanses of Earth's land surface, making them integral components of the cryosphere in terms of past climate and atmospheric proxies, surface albedo regulators, insulators for other Arctic environments and habitats for diverse microbial communities such as algae, bacteria and fungi. Yet, most of our current understanding of snow pack environments, specifically microbial activity and community interaction, is limited to the main microbial growing season during spring ablation. At present, little is known about microbial activity and its influence on nutrient cycling during the subfreezing temperatures and 24-h darkness of the polar winter. Here, we examined microbial dynamics in a simulated cold (-5°C), dark snow pack to determine polar winter season microbial activity and its dependence on critical nutrients. Snow collected from Ny-Ålesund, Svalbard was incubated in the dark over a 5-week period with four different nutrient additions, including glacial mineral particles, dissolved inorganic nitrogen (DIN), dissolved inorganic phosphorus (DIP) and a combined treatment of DIN plus DIP. Data indicate a consumption of dissolved inorganic nutrients, particularly DIN, by heterotrophic communities, suggesting a potential nitrogen limitation, contradictory to phosphorus limitations found in most aquatic environments. 16S amplicon sequencing also reveal a clear difference in microbial community composition in the particulate mineral treatment compared to dissolved nutrient treatments and controls, suggesting that certain species of heterotrophs living within the snow pack are more likely to associate with particulates. Particulate phosphorus analyses indicate a potential ability of heterotrophic communities to access particulate sources of phosphorous, possibly explaining the lack of phosphorus limitation. These findings have importance for understanding microbial activity during the polar winter season and its potential influences on the abundance and bioavailability of nutrients released to surface ice and downstream environments during the ablation season.

Algal photophysiology drives darkening and melt of the Greenland Ice Sheet.

Blooms of Zygnematophycean "glacier algae" lower the bare ice albedo of the Greenland Ice Sheet (GrIS), amplifying summer energy absorption at the ice surface and enhancing meltwater runoff from the largest cryospheric contributor to contemporary sea-level rise. Here, we provide a step change in current understanding of algal-driven ice sheet darkening through quantification of the photophysiological mechanisms that allow glacier algae to thrive on and darken the bare ice surface. Significant secondary phenolic pigmentation (11 times the cellular content of chlorophyll a) enables glacier algae to tolerate extreme irradiance (up to ∼4,000 µmol photons⋅m-2⋅s-1) while simultaneously repurposing captured ultraviolet and short-wave radiation for melt generation. Total cellular energy absorption is increased 50-fold by phenolic pigmentation, while glacier algal chloroplasts positioned beneath shading pigments remain low-light-adapted (Ek ∼46 µmol photons⋅m-2⋅s-1) and dependent upon typical nonphotochemical quenching mechanisms for photoregulation. On the GrIS, glacier algae direct only ∼1 to 2.4% of incident energy to photochemistry versus 48 to 65% to ice surface melting, contributing an additional ∼1.86 cm water equivalent surface melt per day in patches of high algal abundance (∼104 cells⋅mL-1). At the regional scale, surface darkening is driven by the direct and indirect impacts of glacier algae on ice albedo, with a significant negative relationship between broadband albedo (Moderate Resolution Imaging Spectroradiometer [MODIS]) and glacier algal biomass (R2 = 0.75, n = 149), indicating that up to 75% of the variability in albedo across the southwestern GrIS may be attributable to the presence of glacier algae.

Cell membrane fatty acid and pigment composition of the psychrotolerant cyanobacterium Nodularia spumigena CHS1 isolated from Hopar glacier, Pakistan.

In the present study, cyanobacterium isolate CHS1 isolated from Hopar glacier, Pakistan, was analyzed for the first time for cell membrane fatty acids and production of pigments. Sequencing of the 16-23S intergenetic region confirmed identification of the isolate CHS1 as Nodularia spumigena. All chlorophyll and carotenoid pigments were quantified using high-performance liquid chromatography and experiments to test tolerance against a range of physico-chemical conditions were conducted. Likewise, the fatty acid profile of the cell membrane CHS1 was analyzed using gas chromatography and mass spectroscopy. The cyanobacterium isolate CHS1 demonstrated tolerance to 8 g/L% NaCl, 35°C and pH 5-9. The characteristic polyunsaturated fatty acid (PUFA) of isolate CHS1, C18:4, was observed in fatty acid methyl esters (FAMEs) extracted from the cell membrane. CHS1 was capable of producing saturated fatty acids (SFA) (e.g., C16:0), monounsaturated fatty acids (MUFA) (e.g., C18:1) and polyunsaturated fatty acids (e.g., C20:5) in the cell membrane. In this study, we hypothesize that one mechanism of cold adaptation displayed by isolate CHS1 is the accumulation of high amounts of PUFA in the cell membrane.

Glacier Algae: A Dark Past and a Darker Future.

"Glacier algae" grow on melting glacier and ice sheet surfaces across the cryosphere, causing the ice to absorb more solar energy and consequently melt faster, while also turning over carbon and nutrients. This makes glacier algal assemblages, which are typically dominated by just three main species, a potentially important yet under-researched component of the global biosphere, carbon, and water cycles. This review synthesizes current knowledge on glacier algae phylogenetics, physiology, and ecology. We discuss their significance for the evolution of early land plants and highlight their impacts on the physical and chemical supraglacial environment including their role as drivers of positive feedbacks to climate warming, thereby demonstrating their influence on Earth's past and future. Four complementary research priorities are identified, which will facilitate broad advances in glacier algae research, including establishment of reliable culture collections, sequencing of glacier algae genomes, development of diagnostic biosignatures for remote sensing, and improved predictive modeling of glacier algae biological-albedo effects.

Photoecology of the Antarctic cyanobacterium Leptolyngbya sp. BC1307 brought to light through community analysis, comparative genomics and in vitro photophysiology.

Cyanobacteria are important photoautotrophs in extreme environments such as the McMurdo Dry Valleys, Antarctica. Terrestrial Antarctic cyanobacteria experience constant darkness during the winter and constant light during the summer which influences the ability of these organisms to fix carbon over the course of an annual cycle. Here, we present a unique approach combining community structure, genomic and photophysiological analyses to understand adaptation to Antarctic light regimes in the cyanobacterium Leptolyngbya sp. BC1307. We show that Leptolyngbya sp. BC1307 belongs to a clade of cyanobacteria that inhabits near-surface environments in the McMurdo Dry Valleys. Genomic analyses reveal that, unlike close relatives, Leptolyngbya sp. BC1307 lacks the genes necessary for production of the pigment phycoerythrin and is incapable of complimentary chromatic acclimation, while containing several genes responsible for known photoprotective pigments. Photophysiology experiments confirmed Leptolyngbya sp. BC1307 to be tolerant of short-term exposure to high levels of photosynthetically active radiation, while sustained exposure reduced its capacity for photoprotection. As such, Leptolyngbya sp. BC1307 likely exploits low-light microenvironments within cyanobacterial mats in the McMurdo Dry Valleys.

Photoacclimation by Arctic cryoconite phototrophs.

Cryoconite is a matrix of sediment, biogenic polymer and a microbial community that resides on glacier surfaces. The phototrophic component of this community is well adapted to this extreme environment, including high light stress. Photoacclimation of the cryoconite phototrophic community on Longyearbreen, Svalbard, was investigated using in situ variable chlorophyll fluorescence. Rapid light curves (RLCs) and induction-recovery curves were used to analyse photosystem II quantum efficiency, relative electron transport rate and forms of downregulation including non-photochemical quenching (NPQ) and state transitions in cyanobacteria. Phototrophs used a combination of behavioural and physiological photochemical downregulation. Behavioural downregulation is hypothesised to incorporate chloroplast movement and cell or filament positioning within the sediment matrix in order to shade from high light, which resulted in a lack of saturation of RLCs and hence overestimation of productivity. Physiological downregulation likely consisted of biphasic NPQ, comprising a steadily induced light-dependent form and a light-independent NPQ that was not reversed with decreasing light intensity. State transitions by cyanobacteria were the most likely physiological downregulation employed by cyanobacteria within the mixed phototroph community. These findings demonstrate that cryoconite phototrophs combine multiple forms of physiological and behavioural downregulation to optimise light exposure and maximise photosynthetic productivity. This plasticity of photoacclimation enables them to survive productively in the high-light stress environment on the ice surface.

Response of Antarctic cryoconite microbial communities to light.

Microbial communities on polar glacier surfaces are found dispersed on the ice surface, or concentrated in cryoconite holes and cryolakes, which are accumulations of debris covered by a layer of ice for some or all of the year. The ice lid limits the penetration of photosynthetically available radiation (PAR) to the sediment layer, since the ice attenuates up to 99% of incoming radiation. This suite of field and laboratory experiments demonstrates that PAR is an important control on primary production in cryoconite and cryolake ecosystems. Increased light intensity increased efficiency of primary production in controlled laboratory incubations of debris from the surface of Joyce Glacier, McMurdo Dry Valleys, Antarctica. However, when light intensity was increased to levels near that received on the ice surface, without the protection of an ice lid, efficiency decreased and measurements of photophysiology showed that the communities suffered light stress. The communities are therefore well adapted to low light levels. Comparison with Arctic cryoconite communities, which are typically not covered by an ice lid for the majority of the ablation season, showed that these organisms were also stressed by high light, so they must employ strategies to protect against photodamage.

The future of the northeast Atlantic benthic flora in a high CO2 world.

Seaweed and seagrass communities in the northeast Atlantic have been profoundly impacted by humans, and the rate of change is accelerating rapidly due to runaway CO2 emissions and mounting pressures on coastlines associated with human population growth and increased consumption of finite resources. Here, we predict how rapid warming and acidification are likely to affect benthic flora and coastal ecosystems of the northeast Atlantic in this century, based on global evidence from the literature as interpreted by the collective knowledge of the authorship. We predict that warming will kill off kelp forests in the south and that ocean acidification will remove maerl habitat in the north. Seagrasses will proliferate, and associated epiphytes switch from calcified algae to diatoms and filamentous species. Invasive species will thrive in niches liberated by loss of native species and spread via exponential development of artificial marine structures. Combined impacts of seawater warming, ocean acidification, and increased storminess may replace structurally diverse seaweed canopies, with associated calcified and noncalcified flora, with simple habitats dominated by noncalcified, turf-forming seaweeds.

Toxicity of synthetic pyrethroid insecticides to the grass shrimp, Palaemonetes pugio, parasitized with the bopyrid isopod, Probopyrus pandalicola.

The grass shrimp, Palaemonetes pugio, plays a large role in the marine ecosystem, serving as a vital link in the food web between many other species. Marine parasites such as the bopyrid isopod, Probopyrus pandalicola, reduce shrimp growth and reproductive output and may also cause P. pugio to be more vulnerable to the lethal effects of contaminants. The purpose of this study was to determine the toxicity of resmethrin and bifenthrin on the grass shrimp, P. pugio, infected with the bopyrid isopod, Probopyrus pandalicola. A 96-h static renewal test was conducted to determine the toxicity of the pyrethroid insecticides resmethrin and bifenthrin to grass shrimp, Palaemonetes pugio, parasitized with the bopyrid isopod, Probopyrus pandalicola. The results were then compared to similar tests utilizing unparasitized P. pugio. Parasitized P. pugio had lower 24-h LC(50) (1.08 microg/L) and 96-h LC(50) (0.43 microg/L) values for resmethrin than unparasitized P. pugio. However, LC(50) ratio tests found that there was no significant difference between parasitized and unparasitized shrimp when affected by resmethrin (p = 0.1751 and 0.1108, respectively). In contrast, an LC(10) ratio test indicated that there was a significant difference between parasitized and unparasitized P. pugio after 96 h (p < 0.0001). When subjected to bifenthrin, parasitized P. pugio had a higher 24-h LC(50) (0.049 microg/L6) than unparasitized P. pugio. The LC(50) ratio test established that the effects of bifenthrin on parasitized P. pugio when compared to unparasitized P. pugio were significantly different at 24 h (p = 0.0065). However, there were no significant differences between parasitized and unparasitized after 96 h (p = 0.4229). In conclusion, both resmethrin and bifenthrin are toxic to the grass shrimp, P. pugio, regardless of parasite presence, and parasitized shrimp may be more susceptible to lower doses of resmethrin (when exposed in the field).