The giant kelp Macrocystis pyrifera forms abundant underwater forests that hosts diverse and dynamic bacterial communities. In the sub-Antarctic Strait of Magellan, while spatial variability is known to influence these associations, the combined effects of temporal variability and intra-thallus differentiation remains poorly understood. In this study, 16S rRNA gene metabarcoding was used to characterize bacterial diversity and composition by comparing communities across two sampling dates (March, late austral summer, and August, austral winter), two different kelp blade types (apical vegetative and basal reproductive sporophylls), and three sampling sites along the Strait of Magellan (Bahía Buzo, San Gregorio and Buque Quemado) which differ in their environmental settings. Bacterial communities were primarily structured by spatial variation among sites, both in terms of richness and composition. Beta diversity analyses revealed strong site-level differentiation in both sampling periods, while blade-type effects on community composition were only evident in August, indicating a date-related modulation of host-associated bacterial assemblages. Alpha diversity showed few differences related with blade types, whereas spatial variation, particularly in bacterial richness, was more pronounced and varied across dates. Furthermore, the global core microbiota was very small, consisting of only a few ubiquitous taxa consistently associated with Macrocystis pyrifera: Persicirhabdus (Verrucomicrobiia), Thalassotalea (Gammaproteobacteria), and an unclassified member of the family Flavobacteriaceae. Beyond this minimal shared core, core composition varied with blade type, sampling site and date, highlighting the combined influence of these factors on kelp-associated bacterial communities from a remote and understudied sub-Antarctic region.
Snow algae are essential primary producers and carbon sinks in the cryosphere. Disentangling the physiological and molecular responses of these organisms to acute abiotic stress induced by snow dynamics is imperative for revealing survival strategies that sustain the snow microbiome under the extreme conditions of polar regions. Here, we examine the tolerance to a short-term (4h) freezing condition (-20°C) in darkness, followed by a recovery period, in the Antarctic snow alga Chlorominima collina. The responses were analyzed in contrast to a light control (2 °C) by integrating chlorophyll fluorescence of PSII, mRNA-sequencing and oxidative stress detection. The treated cells reduced PSII photochemical efficiency and suppressed the light harvesting process. Simultaneously abiotic stress-responsive genes were expressed, suggesting a reprograming of metabolism and processes, orchestrated by key signaling pathways and transcription factors. This profile revealed common elements of states prior to hypometabolism such as the fuel switch from carbohydrate to lipid catabolism, improved defenses, repression of biosynthetic processes, induction of mitophagy and autophagy, and regulation of transcription and translation. These adjustments promoted the maintenance of cellular homeostasis, as evidenced by enrichment of this process and the recovery of PSII efficiency. Therefore, we proposed that the integration of the reduction of efficiency with which PSII captures energy and the regulation of genes involved in the induction of hypometabolism constitutes an adaptive strategy that confers freezing and darkness tolerance at snow algae. Collectively, the observed functional changes may be relevant for understanding the survival and subsequent adaptation of Chlorophyta to the Antarctic snow environment.
Because of its large size and foundational role, the form and function of the giant kelp Macrocystis pyrifera define key responses to the environmental shifts and ecosystem services. The present study compared several morphological, bio-optical and fluorescence-based photobiological traits as well biomass allocation patterns of the kelp in three sites with different environmental settings along the west coast of the sub-Antarctic strait of Magellan. The morpho-functional and bio-optical characteristics of the algae varied between the sites, following differences in underwater light and tidal range between Atlantic (Buque Quemado and San Gregorio) and Pacific (Bahía Buzos) sectors. Traits measured in blades and individual thalli contributed differently to the total variability within the giant kelp populations. The individuals from the intertidal muddy flats from Buque Quemado differed in many traits, especially biomass allocation along the thallus and bio-optics, with respect to the subtidal rocky assemblages from San Gregorio and especially Bahía Buzos. Photosynthetic characteristics revealed shade adaptation with Ek values normally ≤400 μmol m-2 s-1. In San Gregorio, a site with lower water transparency, light requirements coincide with irradiances at depths between 11 and 4 m, while Ek values estimated for Bahía Buzos indicated photosynthesize at depths >20 m.
Physiological and biochemical responses to elevated temperatures were studied in the isomorphic tetrasporophyte (diploid) and gametophyte (haploid) phases of two Antarctic red macroalgal species (Sarcopeltis antarctica, former Gigartina skottsbergii - and Iridaea cordata), assessing whether ploidy affects the responses to extreme and fast warming events. The tetrasporophyte and gametophyte fronds of both species were exposed in the laboratory to 2 °C (control) and 8 °C (warming event) for up to 3 days. Photosynthetic performance and concentrations of chlorophyll a, total carotenoids, and mycosporine-like amino acids (MAAs) were determined. Inter-and intraspecific differences in physiological and biochemical responses to temperature were observed. Temperature increases slightly stimulated photosynthetic activity (Fv/Fm) over 15 % at 8 °C only in gametophytes of both species. Intraspecific variation in the content of MAAs and total carotenoids was also observed, with tetrasporophytes of S. antarctica and gametophytes of I. cordata evidencing a significative 60 % MAA content decrease (accompanied by a slight increase in total carotenoid) at 8 °C. These results highlight the role of carotenoids in the acclimation to elevated temperature and MAA content at the lowest ones. Although some intraspecific differences in the responses of haplo-diplontic life cycle phase were observed, there were low effects of exposure to 8 °C on photochemistry, outlining the physiological tolerance of both ploidy phases of intertidal species to extreme pulses of temperature increases in Antarctica.
Giant kelp (Macrocystis pyrifera) covers large coastal areas along the Comau Fjord (Northern Patagonia), across different environmental gradients that determine its structural complexity. In the present study, we compared the morphological (thallus length and wet biomass, holdfast diameter, blade morphology, etc.) and photochemical characteristics based on PAM chlorophyll fluorescence (Effective Quantum Yield and P-E curve parameters) of six populations along the Comau Fjord distributed in three sectors: Lilihuapi Island (1 population), Cahuelmo (2 populations) sector and Comau Fjord inside (3 populations). The main results indicated that, at an individual level, different structural conformations of M. pyrifera populations where only observed at the mouth of the fjord, where a well-established "kelp forest" was identified. In contrast, in areas inside the fjord, populated by "patches" and narrow "kelp belts", no differences in biomass and thallus length were recorded. However, the morphological differences between individuals of these populations were related with the size of blades, with blade area being larger in the inner parts of the fjord compared to the other sites. Regarding the photochemical characteristics, in general, the algae showed shade adapted features, with algae from Cahuelmo exhibiting higher ETR values and light requirements (Ek) compared to the other sites. These findings indicating large blade area and lower light demands for photochemistry could be related to a photo-acclimation strategy to respond to the light gradients along the fjord, marked by high water column stratification. Here, the presence of high mountains, especially towards the fjord head, determines the degree of exposure and availability of light for photosynthesis. This study is the first morphological and photochemical characterization of natural populations of M. pyrifera in this area of Northern Patagonia and underlines the importance of morpho-functional traits of kelps to endure environmental variability in an understudied area threatened by global climate change and also local anthropogenic activities.
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The short-term effects of UV radiation and low temperature on ultrastructure, photosynthetic activity (measured as the maximal photochemical quantum yield of photosystem II: Fv/Fm), chlorophyll-a (Chl-a) contents, and UV-absorbing compounds on the carpospores of Iridaea cordata from a sub-Antarctic population were investigated. Exposure to both photosynthetically active radiation (PAR) and PAR + UV for 4 h caused ultrastructural modifications in all treatments. Under PAR + UV at 2 °C, a disruption of the chloroplast’s internal organization was observed. Plastoglobuli were often found in carpospores exposed to 2 °C. ‘Electron dense particles’, resembling physodes of brown algae, were detected for the first time in cells exposed to PAR and PAR + UV at 8 °C. Fv/Fm decreased following 4 h exposure at 2 °C under PAR + UV (64%) and PAR (25%). At 8 °C, Fv/Fm declined by 21% only under PAR + UV. The photosynthesis of carpospores previously treated with UV partially recovered after a 4 h exposure under dim light. UV-absorbing compounds were degraded in all radiation and temperature treatments without recovery after a 4 h dim light period. Chl-a did not change, whereas total carotenoids increased under PAR at 8 °C The study indicates that although carpospores of I. cordata exhibit photoprotective mechanisms, UV radiation strongly damages their ultrastructure and physiology, which were exacerbated under low temperatures.
The giant kelp Macrocystis pyrifera is categorized as a keystone species, forming highly productive forests that provide ecosystem services and host a remarkable marine biodiversity of macro and microorganisms. The association of microorganisms with the algae is close and can be functionally interdependent. The Magellan Strait, a natural marine passage between the Atlantic and Pacific oceans, harbours extensive giant kelp forests. However, information related to the diversity of bacterial communities in this region is still scarce. In this study, 16S rRNA gene metabarcoding was used to characterize the diversity and composition of bacterial communities associated with apical blades and sporophylls of M. pyrifera from different sites (Bahía Buzo, San Gregorio, and Buque Quemado). Additionally, data from satellites and reanalysis, as well as tide data, were used to characterize the environmental variability. The findings revealed discernible local variations in bacterial taxa across sampling sites, with consistent dominance of Proteobacteria, Verrucomicrobia, Bacteroidetes, and Planctomycetes. Furthermore, a distinctive bacterial community structure was identified between apical and sporophyll blades of M. pyrifera. This research marks the inaugural characterization of bacterial community diversity and composition associated with M. pyrifera in the remote and understudied sub-Antarctic region of the Magellan Strait.
Ecological stability is crucial for understanding anthropogenic biodiversity loss and its consequences, especially when disturbances affect species that influence numerous others. The giant kelp Macrocystis pyrifera , an iconic foundation species, supports diverse communities on temperate and subpolar coasts. While giant kelp communities in temperate regions have been extensively studied, field-based manipulative research in subpolar latitudes is still limited. We investigated the resistance, resilience, and recovery of a community subjected to experimental giant kelp removal in a sub-Antarctic ecosystem. We simulated pulsed kelp loss caused by destructive storms and monitored the macrobenthic invertebrate understorey for 12 mo. The experimental disturbance elicited varying stability responses of the understorey. Understorey community biomass was strongly resistant to the disturbance but declined gradually (i.e. low resilience), showing incomplete recovery compared to undisturbed communities. Community density (total number of individuals per sample) increased notably following the removal (i.e. weak resistance) but ultimately returned to undisturbed levels (i.e. high resilience and complete recovery). Species composition exhibited low resistance and resilience, and no recovery from the disturbance. Secondary coextinctions of several understorey species accounted for the observed low compositional stability. In contrast to giant kelp communities in temperate latitudes, the slower recovery rates of kelp and the loss of key positive interactions likely contributed to the observed stability responses in this subpolar ecosystem’s invertebrate understorey. By examining the response of a sub-Antarctic understorey community to giant kelp removal, our study enhances our understanding of how foundation species sustain local biodiversity.
At the West Antarctic Peninsula, snow algae blooms are composed of complex microbial communities dominated by green microalgae and bacteria. During their progression, the assembly of these microbial communities occurs under harsh environmental conditions and variable nutrient content due to fast snow melting. To date, it is still unclear what are the ecological mechanisms governing the composition and abundance of microorganisms during the formation of snow algae blooms. In this study, we aim to examine the main ecological mechanisms governing the assembly of snow algae blooms from early stages to colorful stages blooms. The composition of the microbial communities within snow algae blooms was recorded in the West Antarctic Peninsula (Isabel Riquelme Islet) during a 35-day period using 16S rRNA and 18S rRNA metabarcoding. In addition, the contribution of different ecological processes to the assembly of the microbial community was quantified using phylogenetic bin-based null model analysis. Our results showed that alpha diversity indices of the eukaryotic communities displayed a higher variation during the formation of the algae bloom compared with the bacterial community. Additionally, in a macronutrients rich environment, the content of nitrate, ammonium, phosphate, and organic carbon did not play a major role in structuring the community. The quantification of ecological processes showed that the bacterial community assembly was governed by selective processes such as homogenous selection. In contrast, stochastic processes such as dispersal limitation and drift, and to a lesser extent, homogenous selection, regulate the eukaryotic community. Overall, our study highlights the differences in the microbial assembly between bacteria and eukaryotes in snow algae blooms and proposes a model to integrate both assembly processes.
The Antarctic Peninsula is experiencing one of the highest warming rates globally. In polar regions, macroalgae thrive under extreme environmental conditions, which could worsen because of future climate change scenarios, including increased ultraviolet exposure, extremely low light availability, and fluctuating temperatures, particularly in the intertidal zones. To investigate the potential role of photoprotective and antioxidant mechanisms in response to future increases in sea surface temperatures caused by climate change, we conducted laboratory experiments using three intertidal macroalgae model species: Adenocystis utricularis (Ochrophyta, Phaeophyceae), Pyropia endiviifolia (Rhodophyta, Bangiophyceae), and Monostroma hariotii (Chlorophyta, Ulvophyceae). These algae were collected in Punta Artigas (King George Island, Antarctica) and acclimated at 2°C for 48 h. They were then assessed in laboratory experiments for up to 5 days under two treatments: (1) control conditions at 2°C and (2) elevated tem.perature conditions at 8°C, representing the most negative increment in SSTs estimated by the end of the 21st century. Carbon, nitrogen, pigments (chlorophylls and carotenoids), mycosporine-like amino acids (MAAs), and phenolic compounds were quantified after 3 and 5 days of exposure. For M. hariotii, elevated temperatures led to an increase in the C/N ratio, total antioxidant capacity, and levels of nitrogen, total carotenoids, chlorophyll-a, pigments (chlorophyll-b and violaxanthin), and phenolic compounds. For A. utricularis, elevated temperatures led to elevated C/N ratio and levels of chlorophyll-a and carotenoids (fucoxanthin and β-carotene). For P. endiviifolia, elevated temperatures resulted in elevated levels of carotenoids (lutein and β-carotene), phenolic compounds, and MAAs (porphyra-334, shinorine, and palythine). Thus, our study suggests that increasing water temperatures due to global warming can enhance the photoprotective abilities of three Antarctic intertidal macroalgae (M. hariotii, A. utricularis, and P. endiviifolia), with each species showing specific responses.
The increasing temperatures at the West Antarctic Peninsula (Maritime Antarctic) could lead to a higher occurrence of snow algal blooms which are ubiquitous events that change the snow coloration, reducing albedo and in turn exacerbating melting. However, there is a limited understanding of snow algae blooms biodiversity, composition, and their functional profiles, especially in one of the world's areas most affected by climate change. In this study we used 16S rRNA and 18S rRNA metabarcoding, and shotgun metagenomics to assess the diversity, composition, and functional potential of the snow algae blooms bacterial and eukaryotic communities at three different sites of Maritime Antarctic, between different colors of the algae blooms and between seasonal and semi-permanent snowfields. We tested the hypothesis that the functional potential of snow algae blooms is conserved despite a changing taxonomic composition. Furthermore, we determined taxonomic co-occurrence patterns of bacteria and eukaryotes and assessed the potential for the exchange of metabolites among bacterial taxa. Here, we tested the prediction that there are co-occurring taxa within snow algae whose biotic interactions are marked by the exchange of metabolites. Our results show that the composition of snow algae blooms vary significantly among sites. For instance, a higher abundance of fungi and protists were detected in Fildes Peninsula compared with Doumer Island and O'Higgins. Likewise, the composition varied between snow colors and snow types. However, the functional potential varied only among sampling sites with a higher abundance of genes involved in tolerance to environmental stress at O'Higgins. Co-occurrence patterns of dominant bacterial genera such as Pedobacter, Polaromonas, Flavobacterium and Hymenobacter were recorded, contrasting the absence of co-occurring patterns displayed by Chlamydomonadales algae with other eukaryotes. Finally, genome-scale metabolic models revealed that bacteria within snow algae blooms likely compete for resources instead of forming cooperative communities.
Community assembly is the result of both, deterministic and stochastic processes. The former encompasses niche-based local-scale mechanisms such as environmental filtering and biotic interactions; the latter includes ecological drift, probabilistic colonisation, and random extinctions. Using standardised sampling protocols, we show that the spatial variation in species composition (beta diversity) of shallow subtidal macrobenthic communities of sub-Antarctic (Strait of Magellan and Yendegaia Fjord [Beagle Channel]) and Antarctic (Fildes Bay [King George Island, West Antarctic Peninsula]) localities reflects a high contribution of stochastic processes to community assembly. Null model analyses indicated that random sampling from species pools of different sizes drove the observed among-locality differences in incidence- and abundance-based beta diversity. We analysed a normalised stochasticity ratio (NST), which delimits between more deterministic (<50%) and more stochastic (>50%) assembly. NST was notably larger than 50%, with mean values of 69.5% (95% CI = 69.2–69.8%), 62.5% (62.1–62.9%), and 72.8% (72.5–73.2%) in Strait of Magellan, Yendegaia Fjord, and Fildes Bay, respectively. Accordingly, environmental factors, such as depth, seawater temperature, salinity, and underwater light penetration, accounted for a small fraction of the spatial variation in community composition across the three localities. In this region, therefore, stochastic processes could have stronger effects on community assembly than deterministic niche-based factors. As anthropogenic biotic homogenisation continues apace, our study can give useful insights into the major ecological processes in Southern Ocean’ coastal marine communities.
Snow algae play crucial roles in cold ecosystems, however, many aspects related to their biology, adaptations and especially their diversity are not well known. To improve the identification of snow algae from colored snow, in the present study we used a polyphasic approach to describe a new Antarctic genus, Chlorominima with the species type Chlorominima collina. This new taxon was isolated of colored snow collected from the Collins Glacier (King George Island) in the Maritime Antarctic region. Microscopy revealed biflagellated ellipsoidal cells with a rounded posterior end, a C-shaped parietal chloroplast without a pyrenoid, eyespot, and discrete papillae. Several of these characteristics are typical of the genus Chloromonas, but the new isolate differs from the described species of this genus by the unusual small size of the cells, the presence of several vacuoles, the position of the nucleus and the shape of the chloroplast. Molecular analyzes confirm that the isolated alga does not belong to Chloromonas and therefore forms an independent lineage, which is closely related to other unidentified Antarctic and Arctic strains, forming a polar subclade in the Stephanosphaerinia phylogroup within the Chlamydomonadales. Secondary structure comparisons of the ITS2 rDNA marker support the idea that new strain is a distinct taxon within of Caudivolvoxa. Physiological experiments revealed psychrophilic characteristics, which are typical of true snow algae. This status was confirmed by the partial transcriptome obtained at 2°C, in which various cold-responsive and cryoprotective genes were identified. This study explores the systematics, cold acclimatization strategies and their implications for the Antarctic snow flora.
Early stages of macroalgae are known to be more vulnerable to changes in the abiotic environment than their adult phases. However, in algal groups attaining intricate life-cycles, the ecophysiological responses of haploid and diploid propagules have not been sufficiently studied. In the present study, stress responses of haploid tetraspores and diploid carpospores of sub-Antarctic red alga Mazzaella laminarioides exposed to ultraviolet (UV) radiation were studied. We tested the hypothesis that UV stress responses of two types of spores attaining similar size are determined by light use characteristics by comparing the photobiological and bio-optical traits. Fluorescence-based photosynthetic efficiency was measured during a 5- h exposure and after a 5- h recovery. Germination and growth of spores exposed to UV treatments were also assessed. Diploid carpospores exhibited higher chlorophyll a content and higher absorption in the UV band than tetraspores. Although the maximal quantum yield was higher in carpospores than tetraspores, no differences in light demands were detected. Exposure to photosynthetically active radiation (PAR) caused inhibition of photosynthetic activity only in carpospores (43%), while exposure to a combination of PAR + UV reduced the maximal quantum yield significantly in tetraspores (36%) and carpospores (60%). In both types of spores, a recovery from UV stress was observed, allowing their germination and further development. The different responses to radiation found in haploid and diploid propagules highlight the ecophysiological versatility of different life-cycle phases to cope with light stress factors ensuring finally successful recruitment and survival.
The Antarctic Peninsula is one of the regions to be most affected by increase in sea surface temperatures (SSTs) mediated by Global Climate Change; indeed, most negative predictions imply an up to 6 °C increment by the end of the XXI century. Temperature is one of the most important factors mediating diversity and distribution of macroalgae, although there is still no consensus as to the likely effects of higher SSTs, especially for polar seaweeds. Some available information suggests that potential strategies to withstand future increases in SSTs will be founded upon the glutathione-ascorbate cycle and the induction of chaperone-functioning heat shock proteins (HSPs); however, their eventual role, even for general stress responses, is unclear. The intertidal green, brown and red macroalgae species Monostroma hariotii, Adenocystis utricularis and Pyropia endiviifolia, respectively, from King George Island, Antarctic Peninsula, were exposed to 2 °C (control) and 8 °C (climate change scenario) for up to 5 days (d). Photosynthetic activity (αETR and ETRmax, and EkETR), photoinhibition (Fv/Fm) and photoprotection processes (αNPQ, NPQmax, and EkNPQ) provided no evidence of negative ecophysiological effects. There were moderate increases in H2O2 production and levels of lipid peroxidation with temperature, results supported by stable levels of total glutathione and ascorbate pools, with mostly higher levels of reduced ascorbate and glutathione than oxidized forms in all species. Transcripts of P. endiviifolia indicated a general upregulation of all antioxidant enzymes and HSPs genes studied under warmer temperature, although with different levels of activation with time. This pioneering investigation exploring different levels of biological organization, suggested that Antarctic intertidal macroalgae may be able to withstand future rise in SSTs, probably slightly altering their latitudinal distribution and/or range of thermal tolerance, by exhibiting robust glutathione-ascorbate production and recycling, as well as the induction of associated antioxidant enzymatic machinery and the syntheses of HSPs.