Carlos Rochera

Temperature effects on carbon and nitrogen metabolism in some Maritime Antarctic freshwater phototrophic communities

Biofilms growing on ice and benthic mats are among the most conspicuous biological communities in Antarctic landscapes and harbour a high diversity of organisms. These communities are consortia that make important contributions to carbon and nitrogen input in non-marine Antarctic ecosystems. Here, we study the effect of increasing temperatures on the carbon and nitrogen metabolism of two benthic communities on Byers Peninsula (Livingston Island, Maritime Antarctica): a biofilm dominated by green algae growing on seasonal ice, and a land-based microbial mat composed mainly of cyanobacteria. Inorganic carbon photoassimilation, urea and nitrate uptake and N2-fixation (acetylene reduction activity) rates were determined in situ in parallel at five different temperatures (0, 5, 10, 15, 25°C) using thermostatic baths. The results for the cyanobacterial mat showed that photosynthesis and N2-fixation responded positively to increased temperatures, but urea and NO3− uptake rates did not show a significant variation related to temperature. This microbial mat exhibits relatively low activity at 0°C whereas at higher temperatures (up to 15°C), N2-fixation rate increased significantly. Similarly, the maximum photosynthetic activity increased in parallel with temperature and showed no saturation up to 25°C. In contrast, the ice biofilm displayed higher photosynthetic activity at 0°C than at the other temperatures assayed, and it showed elevated photoinhibition at warmer temperatures.

Spatial Dominance and Inorganic Carbon Assimilation by Conspicuous Autotrophic Biofilms in a Physical and Chemical Gradient of a Cold Sulfurous Spring: The Role of Differential Ecological Strategies

The community composition and ecophysiological features of microbial autotrophic biofilms were studied in Fuente Podrida, a cold sulfur spring located in East Spain. We demonstrated how different ecophysiological strategies, such as resistance and/or utilization of sulfide and oxygen, light adaptation, or resistance to high water flow, allow each of the microorganisms described to efficiently colonize several areas within the environmental gradient. In the zone of the spring constantly influenced by sulfide-rich waters, biofilms were formed by purple bacteria, cyanobacteria, and filamentous colorless sulfur bacteria. Purple bacteria showed higher photosynthetic efficiency per pigment unit than cyanobacteria, although they were dominant only in anoxic areas. Two filamentous cyanobacteria, strain UVFP1 and strain UVFP2, were also abundant in the sulfide-rich area. Whereas the cyanobacterial strain UVFP2 shows a strategy based on the resistance to sulfide of oxygenic photosynthesis, strain UVFP1, additionally, has the capacity for sulfide-driven anoxygenic photosynthesis. Molecular phylogenetic analyses cluster the benthic strain UVFP1 with genus Planktothrix, but with no particular species, whereas UVFP2 does not closely cluster with any known cyanobacterial species. The colorless sulfur bacterium Thiothrix sp. extended throughout the zone in which both sulfide and oxygen were present, exhibiting its capacity for chemolithoautotrophic dark carbon fixation. Downstream from the source, where springwater mixes with well-oxygenated stream water and sulfide disappears, autotrophic biofilms were dominated by diatoms showing higher photosynthetic rates than cyanobacteria and, by a lesser extent, by a sulfide-sensitive cyanobacterium (strain UVFP3) well adapted to low light availability, although in the areas of higher water velocity far from the river shore, the dominance shifted to crust-forming cyanobacteria. Both types of microorganisms were highly sensitive to sulfide impeding them from occupying sulfide-rich areas of the spring. Sulfide, oxygen, light availability, and water velocity appear as the main factors structuring the autotrophic community of Fuente Podrida spring.

Heterogeneous vertical structure of the bacterioplankton community in a non-stratified Antarctic lake.

Abstract Bacterial community composition during summer was analysed in surface and bottom waters of the oligotrophic shallow (4.5 m) Lake Limnopolar (Livingston Island, South Shetland Islands, Antarctica), using 16S rRNA gene clone libraries and sequencing. Up to 61% of the 16S rDNA sequences found were closely related to sequences retrieved from lakes, glaciers or polar systems. The distribution of these sequences was not homogeneous, with vertical differences found in both bacterial taxa composition and isolation source of the closest match from GenBank. In the surface sample 86% of the sequences were related to bacteria found in soils, seawater or gut microbiota, probably explained by waterborne transport from the catchment, by wind through sea sprays, or local bird activity. Conversely, in the deep samples, 95% of the sequences were closer to bacteria typically described for lakes, glaciers or polar systems. The presence of benthic mosses covering the bottom of the lake favours a more stable deep layer leading to the existence of this biological heterogeneity through the water column, although the lake does not show physical-chemical stratification in summer. This study illustrates a strong influence of external factors on the microbial ecology of this model Antarctic lake.

Prokaryotic Community in Lacustrine Sediments of Byers Peninsula (Livingston Island, Maritime Antarctica)

Byers Peninsula (Livingston Island, Antarctica), the largest seasonally ice-free region of the Maritime Antarctica, holds a large number of lakes, ponds, and streams. The prokaryotic structure and bacterial diversity in sediment samples collected during the 2008–2009 austral summer from five inland lakes, two coastal lakes, and an estuarine site were analyzed by Catalyzed Reporter Deposition Fluorescence In Situ Hybridization (CARD-FISH) and 16S rRNA 454 tag pyrosequencing techniques, respectively. Differently from inland lakes, which range around the oligotrophic status, coastal lakes are eutrophic environments, enriched by nutrient inputs from marine animals. Although the prokaryotic abundances (estimated as DAPI stained cells) in sediment samples were quite similar among inland and coastal lakes, Bacteria always far dominated over Archaea. Despite the phylogenetic analysis indicated that most of sequences were affiliated to a few taxonomic groups, mainly referred to Proteobacteria, Bacteroidetes, and Actinobacteria, their relative abundances greatly differed from each site. Differences in bacterial composition showed that lacustrine sediments were more phyla rich than the estuarine sediment. Proteobacterial classes in lacustrine samples were dominated by Betaproteobacteria (followed by Alphaproteobacteria, Deltaproteobacteria, and Gammaproteobacteria), while in the estuarine sample, they were mainly related to Gammaproteobacteria (followed by Deltaproteobacteria, Epsilonproteobacteria, Alphaproteobacteria, and Betaproteobacteria). Higher number of sequences of Alphaproteobacteria, Cyanobacteria, Verrucomicrobia, and Planctomycetes were observed in sediments of inland lakes compared to those of coastal lakes, whereas Chloroflexi were relatively more abundant in the sediments of coastal eutrophic lakes. As demonstrated by the great number of dominant bacterial genera, bacterial diversity was higher in the sediments of inland lakes than that in coastal lakes. Ilumatobacter (Actinobacteria), Gp16 (Acidobacteria), and Gemmatimonas (Gemmatimonadetes) were recovered as dominant genera in both inland and coastal lakes, but not in the estuarine sample, indicating that they may be useful markers of Antarctic lakes. The proximity to the sea, the different lake depths and the external or internal origin of the nutrient sources shape the bacterial communities composition in lacustrine sediments of Byers Peninsula.

Structure of planktonic microbial communities along a trophic gradient in lakes of Byers Peninsula, South Shetland Islands

Abstract A systematic limnological survey of water bodies of Byers Peninsula (Livingston Island, South Shetland Islands) was carried out during the summer of 2001/02. Abundances of microbial plankton were determined which allowed a delineation of the pelagic food web structure. We also report the nutrient status of these lakes. We demonstrate the occurrence of a trophic gradient that extended from upland lakes (oligotrophic) to the coastal ones (eutrophic). The study shows that a lakes morphology regulates the relative importance of the pelagic and benthic habitats, whereas nutrient loads mainly determine its trophic status. Yet, some of the variability observed could be also a legacy of the landscape. Photosynthetic pigments analyses by high-performance liquid chromatography of the lake waters revealed a major occurrence of chlorophytes, chrysophytes and diatoms. The chlorophyll a concentrations in lakes in the central plateau were consistently lower (< 2.5 μg l-1) than coastal sites, which were one order of magnitude higher. Numbers of both bacterioplankton and autotrophic picoplankton also increased from inland to coastal sites. However, the relative role of autotrophic picoplankton in the total phytoplankton assemblage decreased with the increase in nutrients loads. Our results show that the trophic status clearly plays a significant role in structuring the pelagic communities of these lakes despite climatic constraints.

Total mercury and methyl-mercury contents and accumulation in polar microbial mats.

Although polar regions are considered isolated and pristine areas, the organisms that inhabit these zones are exposed to global pollution. Heavy metals, such as mercury, are global pollutants and can reach almost any location on Earth. Mercury may come from natural, volcanic or geological sources, or result from anthropogenic sources, in particular industrial or mining activities. In this study, we have investigated one of the most prominent biological non-marine communities in both polar regions, microbial mats, in terms of their Hg and methyl-mercury (MeHg) concentrations and accumulation capacities. The main hypotheses posed argued on the importance of different factors, and to test them, we have measured Hg concentrations in microbial mats that were collected from 6 locations in different ecological situations. For this purpose, the direct anthropogenic impacts, volcanic influences, proximity to the seashore, latitudinal gradients and C contents were investigated. Our results show that, other than the direct anthropogenic influence, none of the other hypotheses alone satisfactorily explains the Hg content in microbial mats. In contrast, the MeHg contents were noticeably different between the investigated locations, with a higher proportion of MeHg on the McMurdo Ice Shelf (Antarctica) and a lower proportion on Ward Hunt Island (High Arctic). Furthermore, our results from in situ experiments indicated that the microbial mats from South Shetland Islands could quickly accumulate (48 h) Hg when Hg dissolved salts were supplied. Over short-term periods, these mats do not transform Hg into MeHg under field conditions.

Geochemistry of streams from Byers Peninsula, Livingston Island

Abstract In January and February 2009, a series of water samples were collected from streams on Byers Peninsula. These samples were analysed for major elements and δ18O to determine the role of lithology and landscape position on stream geochemistry, and to understand better the hydrology (i.e. residence time of water) of these systems. Precipitation chemistry is enriched in Na+, as are the streams located close to the coast. Streams originating from inland locations have much higher percentages of Ca2+. In contrast, Mg2+ varied little, though streams that are in greater contact with volcanic-derived soils have slightly higher concentrations. Anion percentages varied greatly between streams with SO42- ranging from 5% to 45% of the anion composition. Dissolved Si concentrations as high as 141 μM were observed. All these data suggest that active chemical weathering is occurring in this region. A time series over 13 days at one stream showed little variation in major element geochemistry. The δ18O of precipitation samples collected over this same period varied by ∼10‰ while the majority of stream samples varied less than ∼1.5‰. These data indicate that the stream waters represent mixtures of precipitation events, melting snow and water from the subsurface that had gained solutes through chemical weathering.

Stability and endemicity of benthic diatom assemblages from different substrates in a maritime stream on Byers Peninsula, Livingston Island, Antarctica: the role of climate variability

Abstract Diatom assemblages from four different substrates from a stream on Byers Peninsula were analysed during the summer. The substrate type was the main factor explaining the variability in the diatom assemblages. Sandy biofilms showed a higher diversity and a greater number of endemic species. Two main hydrological regimes were observed: 1) a hydrologically unstable period with high variability in stream flow and successive freezing and thawing periods, 2) a late summer hydrologically stable period, characterized by low stream velocity and variability. The structure of the diatom communities was different between the two hydrological periods, although the substrate modulated the difference. The diatom assemblages showed low similarity among the substrates and high dominance of endemic species during early summer. The late summer community showed high dominance of motile cosmopolitan species on all substrate types. As the length of both hydrological regimes would ultimately be driven by climatic variability, the predicted climate warming could reduce overall stream diversity. Hence, subtle changes could alter the length of both hydrological periods. The relationship between diatom species association with different substrates and hydrological regimes could be relevant for tracking past climate variability using diatom palaeorecords.

Vertical structure of bi-layered microbial mats from Byers Peninsula, Maritime Antarctica

Abstract A summer study of the vertical structure of bi-layered microbial mats was carried out on Byers Peninsula (Livingston Island, South Shetland Islands). These benthic communities had a common basic structure that consisted of two distinct layers differing in composition, morphology and colour. Our sampling focused on mats showing more layering, which thrived over moist soils and at the bottom of ponds. The photosynthetic pigments analysis performed by high-performance liquid chromatography demonstrated a major occurrence of cyanobacteria and diatoms on these mats, the former being more abundant in relative terms on the surface and composed by morphospecies grouping into orders Oscillatoriales, Nostocales and Chroococcales. The areal chlorophyll a concentrations were slightly higher in the deeper layer although not significantly. Our microscopic and chemical analyses showed that non-active biomass accumulates at the surface. Hence, the upper layers showed the sheath pigment scytonemin and higher amounts of exopolysaccharides, as a strategy to cope with environmental stress. On the other hand, the basal layer was composed of more active photosynthetic microbiota, which also revealed a more balanced stoichiometry. Here we exemplify how environmental stresses are potentially overcome by physiological mechanisms developed by microbial mats which also shape their vertical structure.

Community structure and photosynthetic activity of benthic biofilms from a waterfall in the maritime Antarctica

Abstract High-energy flowing water habitats such as waterfalls are uncommon in Antarctica, though they may become more regular as temperature increase. Both high spatial and temporal environmental variability is expected on them. The extent of their biological colonization will depend on the amount of ecological strategies displayed by the surrounding biota. We report here a study on phototrophic microbenthic communities inhabiting such environment in a stream on the Byers Peninsula of Livingston Island. Five different biofilms were distinguished by colour, and were located in specific microhabitat types in the waterfall, which flowed down a steep canyon. Photosynthetic pigment content and microscopic observations demonstrated a different assemblage of chlorophytes, cyanobacteria and diatoms among them. Biofilms were not randomly distributed in the stream channel, which may be related to water flow, nutrient availability and moisture. The exopolymeric substances content, stoichiometry and pigment composition varied among biofilms, likely reflecting differences in the water and nutrients availability. The photosynthetic rates were in the range of the observed in previous studies in the site and varied according to the habitat within the stream. Communities dominated by chlorophytes were restricted to the central channel, suggesting adaptation to faster flow regime. However, cyanobacterial biofilms appeared in a great range of environmental conditions. They were rare in the central channel where water flow was greatest, but achieved large biomass stocks on submerged and even exposed sites in the splash zone at the edge of the flowing water. This study shows how Antarctic biofilms can have a large variability in community structure and biomass over short length scales, reflecting the range of microhabitats in this Antarctic waterfall ecosystem, and the potential occurrence of different strategies to overcome fluctuating conditions.