Temperature Ecotypes Research Articles

Marine Synechococcus picocyanobacteria: Light utilization across latitudes

The most ubiquitous cyanobacteria, Synechococcus, have colonized different marine thermal niches through the evolutionary specialization of lineages adapted to different ranges of temperature seawater. We used the strains of Synechococcus temperature ecotypes to study how light utilization has evolved in the function of temperature. The tropical Synechococcus (clade II) was unable to grow under 16 °C but, at temperatures >25 °C, induced very high growth rates that relied on a strong synthesis of the components of the photosynthetic machinery, leading to a large increase in photosystem cross-section and electron flux. By contrast, the Synechococcus adapted to subpolar habitats (clade I) grew more slowly but was able to cope with temperatures <10 °C. We show that growth at such temperatures was accompanied by a large increase of the photoprotection capacities using the orange carotenoid protein (OCP). Metagenomic analyzes revealed that Synechococcus natural communities show the highest prevalence of the ocp genes in low-temperature niches, whereas most tropical clade II Synechococcus have lost the gene. Moreover, bioinformatic analyzes suggested that the OCP variants of the two cold-adapted Synechococcus clades I and IV have undergone evolutionary convergence through the adaptation of the molecular flexibility. Our study points to an important role of temperature in the evolution of the OCP. We, furthermore, discuss the implications of the different metabolic cost of these physiological strategies on the competitiveness of Synechococcus in a warming ocean. This study can help improve the current hypotheses and models aimed at predicting the changes in ocean carbon fluxes in response to global warming.

Unveiling membrane thermoregulation strategies in marine picocyanobacteria.

The wide latitudinal distribution of marine Synechococcus cyanobacteria partly relies on the differentiation of lineages adapted to distinct thermal environments. Membranes are highly thermosensitive cell components, and the ability to modulate their fluidity can be critical for the fitness of an ecotype in a particular thermal niche. We compared the thermophysiology of Synechococcus strains representative of major temperature ecotypes in the field. We measured growth, photosynthetic capacities and membrane lipidome variations. We carried out a metagenomic analysis of stations of the Tara Oceans expedition to describe the latitudinal distribution of the lipid desaturase genes in the oceans. All strains maintained efficient photosynthetic capacities over their different temperature growth ranges. Subpolar and cold temperate strains showed enhanced capacities for lipid monodesaturation at low temperature thanks to an additional, poorly regiospecific Δ9-desaturase. By contrast, tropical and warm temperate strains displayed moderate monodesaturation capacities but high proportions of double unsaturations in response to cold, thanks to regiospecific Δ12-desaturases. The desaturase genes displayed specific distributions directly related to latitudinal variations in ocean surface temperature. This study highlights the critical importance of membrane fluidity modulation by desaturases in the adaptive strategies of Synechococcus cyanobacteria during the colonization of novel thermal niches.

Thermoacclimation and genome adaptation of the membrane lipidome in marine Synechococcus.

The marine cyanobacteria of the genus Synechococcus are important primary producers, displaying a wide latitudinal distribution that is underpinned by diversification into temperature ecotypes. The physiological basis underlying these ecotypes is poorly known. In many organisms, regulation of membrane fluidity is crucial for acclimating to variations in temperature. Here, we reveal the detailed composition of the membrane lipidome of the model strain Synechococcus sp. WH7803 and its response to temperature variation. Unlike freshwater strains, membranes are almost devoid of C18, mainly containing C14 and C16 chains with no more than two unsaturations. In response to cold, we observed a rarely observed process of acyl chain shortening that likely induces membrane thinning, along with specific desaturation activities. Both of these mechanisms likely regulate membrane fluidity, facilitating the maintenance of efficient photosynthetic activity. A comprehensive examination of 53 Synechococcus genomes revealed clade-specific gene sets regulating membrane lipids. In particular, the genes encoding desaturase enzymes, which is a key to the temperature stress response, appeared to be temperature ecotype-specific, with some of them originating from lateral transfers. Our study suggests that regulation of membrane fluidity has been among the important adaptation processes for the colonization of different thermal niches by marine Synechococcus.

Mycelial growth, pathogenicity, aggressiveness and apothecial development of Sclerotinia sclerotiorum isolates from Brazil and the United States in contrasting temperature regimes

ABSTRACT Fungi can adapt to environmental conditions and produce different physiological responses. The aim of this study was to verify the existence of Sclerotinia sclerotiorum temperature ecotypes in isolates from Brazil and the USA. Ten S. sclerotiorum isolates from tropical and subtropical regions of Brazil and six isolates from the USA were used to measure mycelial growth, pathogenicity and aggressiveness on bean, canola and soybean, as well as apothecial formation at contrasting temperatures. For mycelial growth, regardless of the origin, all isolates grew faster at 20°C, compared to 27°C. For pathogenicity and aggressiveness, disease severity was greater at 20°C than at 30°C considering all isolates. As regards apothecial production, only Brazilian isolates were capable of producing apothecia with no preconditioning. After preconditioning at 4°C during 40 days, isolates from Brazil and the USA produced apothecia. None of the 16 isolates was capable of producing apothecia at 30oC after 40 days. Results indicated no adaptation of S. sclerotiorum isolates from Brazil to grow or colonize leaflets at higher temperatures, compared to isolates from the USA. Only sclerotia from S. sclerotiorum isolates from Brazil were capable of germinating carpogenically without preconditioning.

Adaptive thermostability of light-harvesting complexes in marine picocyanobacteria.

Marine Synechococcus play a key role in global oceanic primary productivity. Their wide latitudinal distribution has been attributed to the occurrence of lineages adapted to distinct thermal niches, but the physiological and molecular bases of this ecotypic differentiation remain largely unknown. By comparing six strains isolated from different latitudes, we showed that the thermostability of their light-harvesting complexes, called phycobilisomes (PBS), varied according to the average sea surface temperature at strain isolation site. Comparative analyses of thermal unfolding curves of the three phycobiliproteins (PBP) constituting PBS rods suggested that the differences in thermostability observed on whole PBSs relied on the distinct molecular flexibility and stability of their individual components. Phycocyanin was the least thermostable of all rod PBP, constituting a fragility point of the PBS under heat stress. Amino-acid composition analyses and structural homology modeling notably revealed the occurrence of two amino-acid substitutions, which might have a role in the observed differential thermotolerance of this phycobiliprotein among temperature ecotypes. We hypothesize that marine Synechococcus ancestors occurred first in warm niches and that during the colonization of cold, high latitude thermal niches, their descendants have increased the molecular flexibility of PBP to maintain optimal light absorption capacities, this phenomenon likely resulting in a decreased stability of these proteins. This apparent thermoadaptability of marine Synechococcus has most probably contributed to the remarkable ubiquity of these picocyanobacteria in the ocean.

Connecting thermal physiology and latitudinal niche partitioning in marine Synechococcus

Marine Synechococcus cyanobacteria constitute a monophyletic group that displays a wide latitudinal distribution, ranging from the equator to the polar fronts. Whether these organisms are all physiologically adapted to stand a large temperature gradient or stenotherms with narrow growth temperature ranges has so far remained unexplored. We submitted a panel of six strains, isolated along a gradient of latitude in the North Atlantic Ocean, to long- and short-term variations of temperature. Upon a downward shift of temperature, the strains showed strikingly distinct resistance, seemingly related to their latitude of isolation, with tropical strains collapsing while northern strains were capable of growing. This behaviour was associated to differential photosynthetic performances. In the tropical strains, the rapid photosystem II inactivation and the decrease of the antioxydant β-carotene relative to chl a suggested a strong induction of oxidative stress. These different responses were related to the thermal preferenda of the strains. The northern strains could grow at 10 °C while the other strains preferred higher temperatures. In addition, we pointed out a correspondence between strain isolation temperature and phylogeny. In particular, clades I and IV laboratory strains were all collected in the coldest waters of the distribution area of marine Synechococus. We, however, show that clade I Synechococcus exhibit different levels of adaptation, which apparently reflect their location on the latitudinal temperature gradient. This study reveals the existence of lineages of marine Synechococcus physiologically specialised in different thermal niches, therefore suggesting the existence of temperature ecotypes within the marine Synechococcus radiation.

Influence of temperature and species origin on Fusarium spp. and Microdochium nivale pathogenicity to wheat seedlings

The influence of temperature and species origin on the in vitro growth rate and pathogenicity of Fusarium and Microdochium nivale (F. avenaceum, F. culmorum, F. graminearum, F. poae, and M. nivale) to wheat seedlings was examined. The mycelial growth of Fusarium avenaceum, F. culmorum, F. graminearum, and F. poae was the fastest at 25&amp;deg;C, and of M. nivale at 15&amp;deg;C. The isolates of F. culmorum, F. graminearum and F. poae originating from mountain regions grew significantly faster at 15&amp;deg;C than those from flatland regions. The isolates from flatland regions grew significantly faster at 25&amp;deg;C than those from mountain regions. F. culmorum and F. graminearum were the most pathogenic species to the root development. The retardation of wheat grain germination caused by the tested species was assessed in descending order: F. culmorum, F. graminearum, M. nivale, F. avenaceum, F. poae. The biomass growth retardation at 15&amp;deg;C was assessed in descending order: F. culmorum, F. graminearum, M. nivale, F. avenaceum, F. poae; at 25&amp;deg;C as follows: F. graminearum, F. culmorum, F. avenaceum, M. nivale, F. poae. The isolates of M. nivale and F. poae originating from mountain regions were significantly more pathogenic than those from flatland regions. The results suggest that there exist different temperature ecotypes and pathotypes of Fusarium species and Microdochium nivale across the territory of the Slovak Republic.

Differences in thermal acclimation of chloroplast functioning in two ecotypes of Valonia utricularis (Chlorophyta)

Chloroplast functioning in two temperature ecotypes of the tropical to warm-temperate green macrophyte Valonia utricularis was monitored by measuring chlorophyll a fluorescence parameters. One ecotype from the Mediterranean Sea is, with respect to growth and survival, more cold-adapted and eurythermal than the cold-sensitive and stenothermal ecotype from the Indian Ocean. Short-term temperature responses of the effective quantum yield (ΦDPSII) between 5 and 35°C and the potential for acclimation of photosystem II to suboptimal growth temperatures (15, 18, 20°C) were investigated. When grown at optimal temperature (25°C), the two ecotypes did not differ to a great extent in the short-term temperature response of OPSII, even though the temperature optimum was lower in the Mediterranean compared with the Indian Ocean isolate (26 vs 33°C). In both ecotypes, decreases in ΦPSII were primarily caused by decreases in the efficiency of excitation capture (Fv′/Fm′) and by the decreased fraction of open reaction centres (qP). ΦDPSII declined in both isolates to 20–30% of the maximum when measured at 5°C. However, the ecotypes showed distinct differences in their potential to acclimate to suboptimal growth temperatures. The Indian Ocean ecotype was not capable of cold acclimation and suffered from photoinhibition when grown at 15–20°C, even though it was capable of adjusting its pigment composition, i.e. by decreasing light absorption combined with increasing the capacity for zeaxanthin-induced energy dissipation. The Mediterranean ecotype was capable of acclimating its photosynthetic efficiency to temperatures of 15–20°C, achieving optimal photosynthetic activity at 18–20°C. Changes in Fv′/Fm′ were mainly responsible for the acclimation response of ΦDPSII. It is suggested that acquisition of cold adaptation and the potential for temperature acclimation in populations of the northeast Atlantic/Mediterranean Sea have enabled V. utricularis, a species with a tropical origin, to extend its biogeographic range into warm-temperate regions.

TEMPERATURE REQUIREMENTS FOR GROWTH AND SURVIVAL OF ANTARCTIC RHODOPHYTA1

ABSTRACTThe temperature requirement for growth and the upper survival temperatures (USTs) of 15 Antarctic red algal species collected on King George Island (South Shetland Islands) and Signy Island (South Orkney Islands) were determined. Two groups with different temperature requirements were identified. 1) A “eurythermal” group includes Rhodymenia subantarctica, Phyllophora ahnfeltioides, Gymnogongrus antarcticus, and Rhodochorton purpureum, growing between 0° and 10°C with optimum values at (0°) 5°(l0°)C. The USTs of these species and of Porphyra endiviifolium, Delesseria lancifolia, and Bangia atropurpurea were between 22° and 16°C. These species survived temperatures in a similar range as most endemic Arctic or Arctic/cold‐temperate species but exhibited a lower temperature demand for growth, suggesting an earlier contact with low temperatures than Arctic species. 2) A stenothermal group includes Pantoneura plocamioides, Myriogramme mangini, Ballia callitricha, Phyllophora antarctica, Gigartina skottsbergii, Georgiella confluens, and Plocamium cartilagineum growing at 0° or ≤5°C with optimum values at 0° or 5°C. The USTs of these species and of Phycodrys austrogeorgica were between 14° and 7°C. The species of this group must have had an even earlier contact with the Antarctic cold‐water environment than species of the “eurythermal” group. Gigartina skottsbergii, Georgiella confluens, Plocamium cartilagineum, and Pantoneura plocamioides were probably exposed longer to low temperatures than the other species of this group or Antarctic green and brown algae because they show the lowest temperature requirements so far determined in seaweeds. The results are discussed in the context of present local temperature regimes at the localities where the isolates were collected. Moreover, an attempt was made to explain the geographic distribution of individual species by the temperature requirements determined in this study. Only a few of the distribution limits are determined by temperature growth and/or survival characteristics. In many species (Rhodymenia subantarctica, Ballia callitricha, Gigartina skottsbergii, Bangia atropurpurea, Rhodochorton purpureum, and Plocamium cartilagineum), the development of temperature ecotypes is evident.

Temperature Ecotypes in Seaweeds: Adaptive Significance and Biogeographic Implications

We examined the existence of temperature ecotypes in seaweed species from the North Atlantic Ocean belonging to different biogeographic groups. Temperature ranges for survival, growth and reproduction were determined in culture for a total of 68 isolates belonging to 18 species. From the data, the reproductive seasonality and potential monthly growth yields in situ were estimated, and the adaptive significance of local ecotypes was assessed. Published palaeo-climatic reconstructions of glacial seawater temperatures were used to determine the importance of climatic change for the development of thermal ecotypes. In all cases highest annual growth yields were obtained by the southernmost populations. Although northernmost isolates had improved their growth capacities at low temperatures, local populations are still exposed to severely suboptimal conditions even in midsummer. There was no apparent relationship between the degree of latitudinal displacement during Pleistocene glacial/interglacial cycles and the development of ecotypes. On the other hand, in disjunct parts of the distribution, where populations have been exposed to different types of temperature stress through glacial/interglacial cycles, thermal ecotypes have evolved. In several cold-water species, western Atlantic populations have higher upper temperature limits for reproduction that those from the eastern Atlantic, which enhanced glacial persistence on the American coast. During the glaciation, eastern Mediterranean and Atlantic populations of tropical to warm temperate species were isolated from one another because of the existence of a cold water barrier near Gibraltar. The resultant lack of gene flow, combined with different types of temperature stress on the disjunct refuge populations, has been of major importance for the development of thermal ecotypes in the North Atlantic Ocean.

Growth and reproduction of Scytosiphon lomentaria (Fucophyceae) in relation to temperature in two populations from Denmark

Two strains of Scytosiphon lomentaria from Denmark have been grown under long-day conditions on a temperature-gradient plate. The material from north-west Jutland (strain No. 46) has a reduced prostrate system (a few-celled lump) whereas the other material from the Sound (strain No. S41) has a well-developed crust. This difference plays a significant role in growth and reproductive patterns. Strain No. 46 rapidly produces a great number of cylindrical macrothalli. Within a four-week experimental period, formation of swarmers from plurilocular sporangia on the macrothalli takes place and results in a maximum dry weight of 32.9 mg at 18.2°C. Swarmers from the macrothalli of strain S41 always develop into knot-filamentous or crust-shaped thalli. The development of the macrothalli, therefore, takes a longer time than in strain 46 and the maximum dry weight is only 16.5 mg at 16°C even within an experimental period of six weeks. The reproductive pattern is more complex than in strain 46. The crusts produce unilocular sporangia at temperatures between 16°C and 23.8°C, and function, therefore, as the reproductive system during the summer as macrothalli disappear at temperatures above 18°C both in nature and in culture. Formation of plurilocular sporangia on macrothalli starts when they are from 6–9 weeks old at temperatures between 11°C and 18°C. The temperature range for growth in the two strains also differs: Strain 46 grows from 7.3–24.4°C while strain S41 grows at least from 4–5.1°C to an upper limit of 27.1°C, but lower limit has not been determined precisely in the present experiment. These results indicate that temperature ecotypes exist, even within a limited geographic area.

Temperature ecotypes near the southern boundary of the kelp Laminaria saccharina

Effects of temperature on survival, growth, and photosynthesis were compared for two USA populations of Laminaria saccharina Lamour. One population was located in New York State, near the southern latitudinal boundary of the species in the western North Atlantic. This southern boundary population was exposed to ambient temperatures ≧20°C for about 6 wk each summer. The second population was located in Maine, toward the center of the latitudinal range of the species, and was rarely exposed to temperatures>17°C. sporophytes from the New York (NY) population exhibited greater tolerance of high temperature than plants from the Maine (ME) site. Juvenile sporophytes from the two sites had similar rates of survivorship and growth at temperatures below 20°C, but showed different responses at 20°C in laboratory experiments. NY plants survived and grew for 6 wk at 20°C. ME plants showed negative growth during wk 2 and 100% mortality during wk 3. NY and ME plants held in situ at the NY site during June to September, 1985, also exhibited differential survivorship when ambient temperatures exceeded 20°C. Results of photosynthesis and dark respiration measurements on NY and ME plants grown at various temperatures suggested that the high-temperature tolerance of NY plants was attributable to their ability to maintain positive daily net C-fixation at 20°C. The high-temperature tolerance of the NY plants appeared to be due to genetic adaptation and is probably crucial to the persistence of the species near its southern boundary.

Temperature tolerance and daylength effects in isolates ofScytosiphon lomentaria (Phaeophyceae) of the North Atlantic and Pacific Ocean

Fifteen geographical isolates ofScytosiphon lomentaria were investigated for their daylength response with regard to upright thallus formation, and nineteen isolates for their upper temperature tolerance. Six new day-neutral and two new photoperiodic strains were found. It became evident that day-neutral strains represent a common reaction group in this species, besides the photoperiodic group. The temperature regulation of photoperiodic and day-neutral strains did not show striking differences and it is assumed that temperature regulation may trigger seasonality of occurrrence in this species as well as photoperiod. The upper survival temperature after two weeks of heart stress is 28–29°C in all tested isolates. No temperature ecotypes were found.