Antarctic Green Alga Research Articles

Gene duplication and functional divergence of new genes contributed to the polar acclimation of Antarctic green algae.

The online version contains supplementary material available at 10.1007/s42995-023-00203-z.

High salt-induced PSI-supercomplex is associated with high CEF and attenuation of state transitions

While PSI-driven cyclic electron flow (CEF) and assembly of thylakoid supercomplexes have been described in model organisms like Chlamydomonas reinhardtii, open questions remain regarding their contributions to survival under long-term stress. The Antarctic halophyte, C. priscuii UWO241 (UWO241), possesses constitutive high CEF rates and a stable PSI-supercomplex as a consequence of adaptation to permanent low temperatures and high salinity. To understand whether CEF represents a broader acclimation strategy to short- and long-term stress, we compared high salt acclimation between the halotolerant UWO241, the salt-sensitive model, C. reinhardtii, and a moderately halotolerant Antarctic green alga, C. sp. ICE-MDV (ICE-MDV). CEF was activated under high salt and associated with increased non-photochemical quenching in all three Chlamydomonas species. Furthermore, high salt-acclimated cells of either strain formed a PSI-supercomplex, while state transition capacity was attenuated. How the CEF-associated PSI-supercomplex interferes with state transition response is not yet known. We present a model for interaction between PSI-supercomplex formation, state transitions, and the important role of CEF for survival during long-term exposure to high salt.

Aberrant light sensing and motility in the green alga Chlamydomonas priscuii from the ice-covered Antarctic Lake Bonney

ABSTRACT The Antarctic green alga Chlamydomonas priscuii is an obligate psychrophile and an emerging model for photosynthetic adaptation to extreme conditions. Endemic to the ice-covered Lake Bonney, this alga thrives at highly unusual light conditions characterized by very low light irradiance (<15 μmol m−2 s−1), a narrow wavelength spectrum enriched in blue light, and an extreme photoperiod. Genome sequencing of C. priscuii exposed an unusually large genome, with hundreds of highly similar gene duplicates and expanded gene families, some of which could be aiding its survival in extreme conditions. In contrast to the described expansion in the genetic repertoire in C. priscuii, here we suggest that the gene family encoding for photoreceptors is reduced when compared to related green algae. This alga also possesses a very small eyespot and exhibits an aberrant phototactic response, compared to the model Chlamydomonas reinhardtii. We also investigated the genome and behavior of the closely related psychrophilic alga Chlamydomonas sp. ICE-MDV, that is found throughout the photic zone of Lake Bonney and is naturally exposed to higher light levels. Our analyses revealed a photoreceptor gene family and a robust phototactic response similar to those in the model Chlamydomonas reinhardtii. These results suggest that the aberrant phototactic response in C. priscuii is a result of life under extreme shading rather than a common feature of all psychrophilic algae. We discuss the implications of these results on the evolution and survival of shade adapted polar algae.

An Antarctic Alga That Can Survive The Extreme Cold

Microscopic algae are tougher than you might think. Some can even survive the extreme cold. In this article, we describe one of the coolest algae of all, the Antarctic green alga called Chlamydomonas sp. UWO241. This one-celled super-organism lives deep in the frigid waters of a remote and permanently ice-covered lake in Antarctica. How does this little alga thrive in such a barren and unwelcoming place? Well, dive into this article to learn how studying the genome of UWO241 is helping scientists better understand this amazingly hardy alga.

Microglena antarctica sp. nov. a New Antarctic Green Alga from Inexpressible Island (Terra Nova Bay, Ross Sea) Revealed through an Integrative Approach

One of the aims of the XXXIV Italian Antarctic Expedition is the study of the photosynthetic biodiversity of the Ross Sea. To achieve this goal, sea-ice samples were collected from Inexpressible Island and a strain of a green microalga (IMA076A) was isolated for morphological and molecular investigations. Combining: (1) phylogenetic analyses of the small subunit rDNA (18S rDNA) and of the internal transcribed spacer 2 (ITS-2) sequences; (2) species delimitation methods; (3) comparative analyses of the secondary structures of ITS-2 and compensatory base changes; (4) morphological, ultrastructural and ecological features, we described the strain IMA076A and its relatives as the new species Microglena antarctica sp. nov. The discovery of a new species of Chlorophyceae highlights that the biological diversity of Antarctic microalgae is more extensive than previously thought and that molecular phylogeny together with compensatory base changes (CBCs) approach are pivotal in the identification of cryptic microalgae.

A species by any other name would sound as sweet.

David Smith argues against the prevalent practice of naming newly discovered species after human beings.

A constitutive stress response is a result of low temperature growth in the Antarctic green alga Chlamydomonas sp. UWO241.

The Antarctic green alga Chlamydomonas sp. UWO241 is an obligate psychrophile that thrives in the cold (4-6°C) but is unable to survive at temperatures ≥18°C. Little is known how exposure to heat affects its physiology or whether it mounts a heat stress response in a manner comparable to mesophiles. Here, we dissect the responses of UWO241 to temperature stress by examining its growth, primary metabolome and transcriptome under steady-state low temperature and heat stress conditions. In comparison with Chlamydomonas reinhardtii, UWO241 constitutively accumulates metabolites and proteins commonly considered as stress markers, including soluble sugars, antioxidants, polyamines, and heat shock proteins to ensure efficient protein folding at low temperatures. We propose that this results from life at extreme conditions. A shift from 4°C to a non-permissive temperature of 24°C alters the UWO241 primary metabolome and transcriptome, but growth of UWO241 at higher permissive temperatures (10 and 15°C) does not provide enhanced heat protection. UWO241 also fails to induce the accumulation of HSPs when exposed to heat, suggesting that it has lost the ability to fine-tune its heat stress response. Our work adds to the growing body of research on temperature stress in psychrophiles, many of which are threatened by climate change.

Adaptation to Extreme Antarctic Environments Revealed by the Genome of a Sea Ice Green Alga

The unicellular green alga Chlamydomonas sp. ICE-L thrives in polar sea ice, where it tolerates extreme low temperatures, high salinity, and broad seasonal fluctuations in light conditions. Despite the high interest in biotechnological uses of this species, little is known about the adaptations that allow it to thrive in this harsh and complex environment. Here, we assembled a high-quality genome sequence of ∼542 Mb and found that retrotransposon proliferation contributed to the relatively large genome size of ICE-L when compared to other chlorophytes. Genomic features that may support the extremophilic lifestyle of this sea ice alga include massively expanded gene families involved in unsaturated fatty acid biosynthesis, DNA repair, photoprotection, ionic homeostasis, osmotic homeostasis, and reactive oxygen species detoxification. The acquisition of multiple ice binding proteins through putative horizontal gene transfer likely contributed to the origin of the psychrophilic lifestyle in ICE-L. Additional innovations include the significant upregulation under abiotic stress of several expanded ICE-L gene families, likely reflecting adaptive changes among diverse metabolic processes. Our analyses of the genome, transcriptome, and functional assays advance general understanding of the Antarctic green algae and offer potential explanations for how green plants adapt to extreme environments.

Chlamydomonas sp. UWO 241 Exhibits High Cyclic Electron Flow and Rewired Metabolism under High Salinity.

The Antarctic green alga Chlamydomonas sp. UWO 241 (UWO 241) is adapted to permanent low temperatures, hypersalinity, and extreme shade. One of the most striking phenotypes of UWO 241 is an altered PSI organization and constitutive PSI cyclic electron flow (CEF). To date, little attention has been paid to CEF during long-term stress acclimation, and the consequences of sustained CEF in UWO 241 are not known. In this study, we combined photobiology, proteomics, and metabolomics to understand the underlying role of sustained CEF in high-salinity stress acclimation. High salt-grown UWO 241 exhibited increased thylakoid proton motive flux and an increased capacity for nonphotochemical quenching. Under high salt, a significant proportion of the up-regulated enzymes were associated with the Calvin-Benson-Bassham cycle, carbon storage metabolism, and protein translation. Two key enzymes of the shikimate pathway, 3-deoxy-d-arabinoheptulosonate 7-phosphate synthase and chorismate synthase, were also up-regulated, as well as indole-3-glycerol phosphate synthase, an enzyme involved in the biosynthesis of l-Trp and indole acetic acid. In addition, several compatible solutes (glycerol, Pro, and Suc) accumulated to high levels in high salt-grown UWO 241 cultures. We suggest that UWO 241 maintains constitutively high CEF through the associated PSI-cytochrome b 6 f supercomplex to support robust growth and strong photosynthetic capacity under a constant growth regime of low temperatures and high salinity.

Phylotypic Characterization of Mycobionts and Photobionts of Rock Tripe Lichen in East Antarctica.

Saxicolous rock ripe lichens that grow on rocks in the East Antarctic fellfields were sampled for phylotypic characterization of its constituent mycobionts (fungi) and photobionts (algae and cyanobacteria). The rock tripe lichen-forming fungal and algal phylotypes were classified under the common lichen-forming genera of ascomycetes, namely, Umbilicaria, and green algae, namely, Trebouxia and Coccomyxa. However, phylotypes of the green algal chloroplasts and the lichen-associated cyanobacteria showed unexpectedly high diversity. The detected chloroplast phylotypes were not fully affiliated with the green algal genera Trebouxia or Coccomyxa. The predominant chloroplast phylotype demonstrated maximum resemblance to Neglectella solitaria, which is neither a known Antarctic species nor a typical lichen photobiont. Another dominant chloroplast phylotype belonged to the atypical Antarctic green algae family. Cyanobacterial phylotypes were dominated by those affiliated with the Microcoleus species rather than the well-known lichen-associates, Nostoc species. The occurrences of these Microcoleus-affiliated cyanobacterial phylotypes were specifically abundant within the Yukidori Valley site, one of the Antarctic Specially Protected Areas (ASPA). The ASPA site, along with another 50 km-distant site, yielded most of the cryptic diversity in the phylotypes of chloroplasts and cyanobacteria, which may contribute to the phenotypic variability within the rock tripe lichen photobionts.

Characterization of photosynthetic ferredoxin from the Antarctic alga Chlamydomonas sp. UWO241 reveals novel features of cold adaptation

The objective of this work was to characterize photosynthetic ferredoxin from the Antarctic green alga Chlamydomonas sp. UWO241, a key enzyme involved in distributing photosynthetic reducing power. We hypothesize that ferredoxin possesses characteristics typical of cold-adapted enzymes, namely increased structural flexibility and high activity at low temperatures, accompanied by low stability at moderate temperatures. To address this objective, we purified ferredoxin from UWO241 and characterized the temperature dependence of its enzymatic activity and protein conformation. The UWO241 ferredoxin protein, RNA, and DNA sequences were compared with homologous sequences from related organisms. We provide evidence for the duplication of the main ferredoxin gene in the UWO241 nuclear genome and the presence of two highly similar proteins. Ferredoxin from UWO241 has both high activity at low temperatures and high stability at moderate temperatures, representing a novel class of cold-adapted enzymes. Our study reveals novel insights into how photosynthesis functions in the cold. The presence of two distinct ferredoxin proteins in UWO241 could provide an adaptive advantage for survival at cold temperatures. The primary amino acid sequence of ferredoxin is highly conserved among photosynthetic species, and we suggest that subtle differences in sequence can lead to significant changes in activity at low temperatures.

Acclimation of Antarctic Chlamydomonas to the sea-ice environment: a transcriptomic analysis

The Antarctic green alga Chlamydomonas sp. ICE-L was isolated from sea ice. As a psychrophilic microalga, it can tolerate the environmental stress in the sea-ice brine, such as freezing temperature and high salinity. We performed a transcriptome analysis to identify freezing stress responding genes and explore the extreme environmental acclimation-related strategies. Here, we show that many genes in ICE-L transcriptome that encoding PUFA synthesis enzymes, molecular chaperon proteins, and cell membrane transport proteins have high similarity to the gens from Antarctic bacteria. These ICE-L genes are supposed to be acquired through horizontal gene transfer from its symbiotic microbes in the sea-ice brine. The presence of these genes in both sea-ice microalgae and bacteria indicated the biological processes they involved in are possibly contributing to ICE-L success in sea ice. In addition, the biological pathways were compared between ICE-L and its closely related sister species, Chlamydomonas reinhardtii and Volvox carteri. In ICE-L transcripome, many sequences homologous to the plant or bacteria proteins in the post-transcriptional, post-translational modification, and signal-transduction KEGG pathways, are absent in the nonpsychrophilic green algae. These complex structural components might imply enhanced stress adaptation capacity. At last, differential gene expression analysis at the transcriptome level of ICE-L indicated that genes that associated with post-translational modification, lipid metabolism, and nitrogen metabolism are responding to the freezing treatment. In conclusion, the transcriptome of Chlamydomonas sp. ICE-L is very useful for exploring the mutualistic interaction between microalgae and bacteria in sea ice; and discovering the specific genes and metabolism pathways responding to the freezing acclimation in psychrophilic microalgae.

Analysis of Expressed Sequence Tags from the Antarctic Psychrophilic Green Algae, Pyramimonas gelidicola

Expressed sequence tags (ESTs) from the Antarctic green algae Pyramimonas gelidicola were analyzed to obtain molecular information on cold acclimation of psychrophilic microorganisms. A total of 2,112 EST clones were sequenced, generating 222 contigs and 219 singletons, and 200 contigs and 391 singletons from control (4 degrees C) and cold-shock conditions (-2 degrees C), respectively. The complete EST sequences were deposited to the DDBJ EST database (http:// www.ddbj.nig.ac.jp/index-e.html) and the nucleotide sequences reported in this study are available in the DDBJ/EMBL/ GenBank. These EST databases of Antarctic green algae can be used in a wide range of studies on psychrophilic genes expressed by polar microorganisms.

Cloning and expression analysis of two different LhcSR genes involved in stress adaptation in an Antarctic microalga, Chlamydomonas sp. ICE-L

Light-harvesting complexes (LHCs) play essential roles in light capture and photoprotection. Although the functional diversity of individual LHCs in many plants has been well described, knowledge regarding the extent of this family in the majority of green algal groups is still limited. In this study, two different LhcSR genes, LhcSR1 and LhcSR2 from Chlamydomonas sp. ICE-L, were cloned from the total cDNA and characterized in response to high light (HL), low light (LL), UV-B radiation and high salinity. The lower F (v)/F (m) as well as the associated induction of non-photochemical quenching (NPQ), observed under those conditions, indicated that Chlamydomonas sp. ICE-L was under stress. Under HL stress, the expression of LhcSR1 and LhcSR2 increased rapidly from 0.5h HL and reached a maximum after 3h. In LL, LhcSR2 expression was up-regulated during the first 0.5h after which it decreased, while the expression of LhcSR1 decreased gradually from the beginning of the experiment. In addition, the transcript levels of LhcSR1 and LhcSR2 increased under UV-B radiation and high salinity. These results showed that both genes were inducible and up-regulated under stress conditions. A higher NPQ was accompanied by the up-regulated LhcSR genes, suggesting that LhcSR plays a role in thermal energy dissipation. Overall, the results presented here suggest that LhcSR1 and LhcSR2 play a primary role in photoprotection in Chlamydomonas sp. ICE-L under stress conditions and provide an important basis for investigation of the adaptation mechanism of LhcSR in Antarctic green algae.

Hidden levels of phylodiversity in Antarctic green algae: further evidence for the existence of glacial refugia

Recent data revealed that metazoans such as mites and springtails have persisted in Antarctica throughout several glacial-interglacial cycles, which contradicts the existing paradigm that terrestrial life was wiped out by successive glacial events and that the current inhabitants are recent colonizers. We used molecular phylogenetic techniques to study Antarctic microchlorophyte strains isolated from lacustrine habitats from maritime and continental Antarctica. The 14 distinct chlorophycean and trebouxiophycean lineages observed point to a wide phylogenetic diversity of apparently endemic Antarctic lineages at different taxonomic levels. This supports the hypothesis that long-term survival took place in glacial refugia, resulting in a specific Antarctic flora. The majority of the lineages have estimated ages between 17 and 84 Ma and probably diverged from their closest relatives around the time of the opening of Drake Passage (30-45 Ma), while some lineages with longer branch lengths have estimated ages that precede the break-up of Gondwana. The variation in branch length and estimated age points to several independent but rare colonization events.

IDENTIFICATION OF A PSYCHROPHILIC GREEN ALGA FROM LAKE BONNEY ANTARCTICA: CHLAMYDOMONAS RAUDENSIS ETTL. (UWO 241) CHLOROPHYCEAE1

An unusual psychrophilic green alga was isolated from the deepest portion of the photic zone (&lt;0.1% of incident PAR) at a depth of 17 m in the permanently ice‐covered lake, Lake Bonney, Antarctica. Here we identify and report the first detailed morphological and molecular examination of this Antarctic green alga, which we refer to as strain UWO 241. To determine the taxonomic identity, UWO 241 was examined using LM and TEM and partial sequences of the small subunit (SSU), internal transcribed spacer (ITS) 1 and ITS2 regions (including the 5.8S) of the ribosomal operon. These data were compared with those of previously described taxa. We identified UWO 241 as a strain of Chlamydomonas raudensis Ettl (SAG 49.72). Chlamydomonas raudensis is closely related to C. noctigama Korshikov (UTEX 2289) as well as foraminifer symbionts such as C. hedleyi Lee, Crockett, Hagen et Stone (ATCC 50216). In addition, its morphology, pigment complement, and phototactic response to temperature are reported. Chlamydomonas raudensis (UWO 241) contains relatively high levels of lutein and low chl a/b ratios (1.6±0.15), and the phototactic response was temperature dependent. The Antarctic isolate (UWO 241) included the typical photosynthetic pigments found in all chl a/b containing green algae. It possesses a small eyespot and, interestingly, was positively phototactic only at higher nonpermissive growth temperatures. Comparison of SSU and ITS rDNA sequences confirms the identification of the strain UWO 241 as C. raudensis Ettl and contradicts the previous designation as C. subcaudata Wille.

Metabolic changes of the Antarctic green algaPrasiola crispasubjected to water stress investigated byin vivo31P NMR

The energy status and the phosphate metabolism of Prasiola crisp during and after desiccation stress was investigated by in vivo31P NMR. The effect of desiccation was simulated by addition of the nonionic osmoticum PEG 200 (polyethylene glycol). Photosynthesis and respiration were effectively inhibited under these conditions. The most notable changes in the in vivo31P NMR spectra were an increase in the cytoplasmic inorganic phosphate signal after PEG stress, a decrease in the polyphosphates and a lowfield shift of the core polyphosphate signal followed by an appearance of extracellular inorganic phosphate. Cytoplasmic pH remained almost constant during stress. After a return to control conditions, photosynthesis and respiration recovered within 4 h as well as the concentrations of the phosphorus metabolites. An as yet unassigned phosphate signal increased in the phosphodiester region of the NMR spectra. Simultaneousty, the polyphosphate signal recovered in intensity and chemical shift. It is suggested that phosphate metabolism and complexation of cations to polyphosphates may play an important role in the distinct desiccation tolerance of P. crispa.

Effect of culture temperature shift on the cellular sugar accumulation of Chlorella vulgaris SO-26

Abstract We investigated the effect of culture temperature on the maximum specific growth rate and cellular sugar accumulation, and the effect of a temperature shift on the sugar accumulation of cells of an Antarctic green alga, Chlorella vulgaris SO-26, in a batch culture system. Decreases in temperature appeared to correlate with decreases in the maximum specific growth rate; on the other hand, the cellular sugar content showed a reverse tendency against temperature. We attempted to use this tendency to improve sugar productivity in Chlorella. First, we cultured Chlorella at 20°C during the logarithmic growth phase to obtain a high specific growth rate. The culture temperature was then shifted from 20°C to 14°C during the stationary growth phase to increase the cellular sugar content. As a result, we obtained a 25% increase in sugar production over that obtained by culture at 20°C throughout the culture.

Physiology and Ultrastructure of Desiccation in the Green Alga Prasiola crispa from Antarctica

Physiological and fine structural responses of the antarctic green alga Prasiola crispa ssp. antarctica (Kutz.) Knebel to desiccation and reimmersion in seawater are described. Experiments were conducted in the dark over a 14 day period, using a range of relative humidities (5% to 95%). Emersed thalli lost about 75% of the total cellular water during 6 hours of desiccation. Maximum water loss (86%) occurred after 1 day exposure to 50% relative humidity (r. h.), and then remained stable for 14 days. Water loss of more than 90% led to irreversible damage of the plants (...)

The effect of light intensity and daylength on the β‐dimethylsulphoniopropionate (DMSP) content of marine green macroalgae from Antarctica*

Abstract. The β‐dimethylsulphoniopropionate (DMSP) concentrations of 5 Antarctic green algae grown at 2, 30 and 55 μmol photons m−2 s−1 were determined during a period of one year, cultivated under fluctuating daylengths mimicking the conditions of the natural habitat at King George Island. Antarctica. The intracellular DMSP content of all species decreased simultaneously with decreasing daylengths and vice versa. Additionally, the DMSP level was affected by the light intensity: the higher the photon fluence rate the greater the algal DMSP concentration. Under conditions of darkness, there was a degradation of the DMSP pool in members of the Acrosiphoniales, while the DMSP content in members of the Ulvales did not change. The results indicate a light‐dependent DMSP accumulation in algae. Therefore, they may help to explain the seasonal variability of DMSP and its cleavage product dimethylsulphide (DMS) in coastal waters.