Cyanobacterial diversity and dominance in polar aquatic ecosystems

1Centre for Northern Studies (CEN) & Dépt de Biologie, Laval University, Québec City, Canada2 Dpto de Biología, Universidad Autónoma de Madrid, Madrid, Spain

WARWICK F. VINCENT 1 & ANTONIO QUESADA2

Online with Ecology of Cyanobacteria II (Chap. 27)Whitton BA (ed.) (2012) Springer, Dordrecht.Images (other than those acknowledged) copyright of authors of article

CONTENTS

Introduction 3Picocyanobacteria 7 Mat-forming cyanobacteria 13

Nostoc communities 14Oscillatorian mats 15Pigments 16Light capture and photosynthesis 19Biodiversity 20The cold biosphere 21

References 22

Supplemental material :Video 1Video 2

All images and videos are reproduced with permission; individual acknowledgements with images

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But the botanist on Nordenskiöld’s team in his epic traverse across the Greenland Ice Cap discovered “cryoconite holes”: cylindrical holes ablated into the ice. They were filled with sediment, water and cyanobacteria. Later studies showed that these communities contained several cyanobacterial taxa and were dominated by the nitrogen-fixing species Calothrix parietina.

IntroductionEarly explorers in the Arctic noted the unexpected presence of cyanobacteria

"Greenland: a tract, perhaps the only one in the world, that was a perfect desert as regards botany"

Nordenskiöld (in Leslie 1879)

Similarly, explorers to Antarctica provided evidence of cyanobacteria. For example, Scott’s expedition (1910-13) to Ross Island and the McMurdo Dry Valleys (shown here) brought back samples and accounts of “water plants” (cyanobacteria) growing beneath the ice in meltwater lakes.

Drawings of cyanobacteria collected from Ross Island, Antarctica (latitude 77°S) during Scott’s Terra Nova expedition. The newly described taxa were Phormidium priestleyi (16), Schizothrix antarctica (21-24) and Nostoc fuscens var. mixta (25-31). From Plate I in Fritsch (1917), from Vincent (2000).

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High latitude cyanobacteriaMost of the aquatic taxa fall into three main ecological groups (Vincentand Quesada 2012):

1) Picocyanobacteria These cells are typically around 1 µm in cross-sectional diameter, and their high surface-to-volume ratio makes them especially well suited to oligotrophic waters. Given the low nutrient status of most high latitude lakes and rivers, picocyanobacteria are widely distributed and abundant in the aquatic ecosystems of both polar regions, as expected. In some environments these occur in colonial form.

2) Gas-vacuolate bloom-formers Genera such as as Anabaena, Microcystis and Aphanizomenon are rare in the polar regions. However, naturally enriched lakes in the subarctic have been found to contain blooms of Anabaena and Oscillatoria.

3) Phytobenthos.= The most abundant cyanobacterial communities in the polar regions are those forming mats, films and crusts over the bottom substrata of lakes, ponds, streams and other aquatic ecosystems.

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Samples from ice-covered Lake A in the Canadian High Arctic under light (left) and epifluorescence (right) microscopy.

Picocyanobacteria In many Arctic and Antarctic lakes, picocyanobacteria are the most abundant photosynthetic cell type in the plankton. These cells are too small to be enumerated by light microscopy, but they are readily observed and counted by their fluorescence under green light.

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Picocyanobacteria and the Cold Ocean Anomaly

Picocyanobacteria are often present in high concentrations in polar lakes and rivers. Highest concentrations have been measured in cold, meromictic (permanently stratified) Ace Lake, Vestfold Hills, Antarctica, where populations rise to 1010 cells L-1.

Despite their ecological success in perennially cold Arctic and Antarctic lakes, picocyanobacteria are anomalously rare or absent from polar oceans. Examples include:

• Picocyanobacteria in epishelf lakes (freshwater versus ocean)

• Picocyanobacterial gradients in Arctic rivers and estuaries

• The Arctic Ocean picocyanobacterial desert

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Milne Fiord - 13 July 2007

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Picocyanobacteria in Arctic fjords - 1Picocyanobacteria occur in the surface freshwaters of Milne Fjord epishelf lake in the Canadian High Arctic, but are present in only low concentrations in the underlying seawater.

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Picocyanobacteria in Arctic fjords - 2Picocyanobacteria occur in the surface freshwaters of Milne Fjord epishelf lake in the Canadian High Arctic, but are present in only low concentrations in the underlying seawater.

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Picocyanobacteria in riversPicocyanobacteria also occur in large Arctic rivers. In the Mackenzie River (shown below), in the Northwest Territories of Arctic Canada, concentrations of picocyanobacteria decline precipitously across the estuarine transition from around 50,000 cells mL-1 in the freshwaters of the river to around 30 cells mL-1 in the coastal Beaufort Sea (Vallières et al. 2008).

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Picocyanobacteria in the Arctic OceanPicocyanobacterial concentrations in the world ocean decline precipitously with increasing latitude North or South (Vincent 2000). This summer 2008 transect from the North Pacific Ocean across the Arctic Ocean and into the North Atlantic Ocean shows the paucity of cells throughout the Arctic Ocean (W.K.W. Li & C. Lovejoy, unpublished), where the picophytoplankton is dominated by microbial eukaryotes, specifically picoprasinophytes (Lovejoy et al. 2007).

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Mat-forming cyanobacteriaCyanobacteria form extensive microbial mats in Arctic and Antarctic lakes, ponds and streams where they may dominate the total ecosystem biomass and productivity. The mats shown here were photographed in a pond at Cape Discovery at the northern coastline of Ellesmere Island in the Canadian High Arctic.

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Mat-forming cyanobacteria - NostocMats and colonies of nitrogen-fixing Nostoc are common in freshwater habitats in both polar regions. Black Nostoc mats rich in the UV-screening pigment scytonemin occur over the delta of Canada Stream in the McMurdo Dry Valleys, Antarctica (left). Spherical colonies as well as cohesive sheets of Nostoc occur in lakes and ponds in the Arctic, and contain abundant heterocysts (right, from a spherical colony in a lake on Ellesmere Island, Canada).

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Mat-forming cyanobacteria - OscillatoriansMany polar cyanobacterial mats are composed largely of oscillatorian cyanobacteria, especially of the genera Oscillatoria, Leptolyngybya, Pseudanabaena and Phormidium. These filamentous taxa and the extracellular polymeric substances (EPS) that they excrete form a cohesive matrix (SEM micrograph at left) that may contain large amounts of particulate mineral material. In shallow waters, the mats have a layered structure that has high concentrations of photoprotective carotenoids at the surface such as canthaxanthin and myxoxanthophyll, and high concentrations of light-capturing pigments in the lower layer, such as chlorophyll a and phycobiliproteins.

Carotenoid-rich surface layer: orange, red, brown.

Chlorophyll- & phycocyanin- rich bottom layer where most of the photosynthesis is localised.

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Mat-forming cyanobacteria -pigmentsThese examples of oscillatorian mats are from lakes in the vicinity of Syowa Station, in East Antarctica. The cyanobacteria included Leptolyngbya perelegans, Leptolyngbya tenuis and Nostoc sp. Green algae were also well represented in the mats, including desmids and the genera Thorakochloris, Kentrosphaera and Oedogonium. The mats had high concentrations of photoprotective pigments, and low overall photosynthetic efficiencies (Tanabe et al. 2010).

From Tanabe et al. (2010)

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Mat-forming cyanobacteria -pigmentsOscillatorian mats also occur at the bottom of deep Antarctic lakes, and were first observed in the meromictic lakes of the McMurdo Dry Valleys (Wharton et al. 1983). Research divers entered the lakes via holes that were melted through 3-5 m of perennial ice and discovered luxuriant mat communities, some of which are calcified and forming ‘living stromatolites’. The communities are often pink in color as a result of high concentrations of phycoerythrin.

Video-1 (supplemental material): Diver returning to the surface through the access hole.

Video-2 (supplemental material): Diver sampling the benthic cyanobacterial mats in Lake Joyce, McMurdo Dry Valleys.

Videocredits: Dale T Andersen, all rights reserved

Left The length of auger required to penetrate the ice at Lake Vanda for sampling by water bottle (photocredit: Antarctica New Zealand). Right The hole melted in the lake ice for diving access. (photocredit: Dale T Andersen).

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Mat-forming cyanobacteria pigmentsThe mat community in Lake Untersee, East Antarctica, produces phycoerythrin-rich conical structures that extend up to 50 cm above the lake floor. The communities are dominated by Phormidium spp., and the structures have laminations of fine clays and organic material that appear to represent decadal time scales (Andersen et al. 2011). Photocredit: D.T. Andersen.

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Mat-forming cyanobacteria – light capture and photosynthesisThe microbial mats have a high light-capturing ability, and the deep-living mats show high photosynthetic efficiencies. In situ studies on the benthic mats in the McMurdo Dry Valley lakes showed that they have photosynthetic quantum yields that approach the theoretical maximum of 1 mole of O2 released for 8 moles of photons absorbed (Hawes & Schwartz 2001).

Laboratory studies of polar oscillatorian taxa in culture have shown that their pigments and light absorption properties change in response to the irradiance levels during culture, but to an extent that varies greatly among taxa. The light absorption per unit cell of the thin filaments of these mats can be as high as that for picocyanobacteria. In this experiment (shown on left) cultures of Antarctic and Arctic oscillatorians (E1-E5) and picocyanobacteria (P1-P4) were incubated for 5 days at 700 (heavy bottom line), 100 and 20 (top line) µmol photon m-2 s-1 prior to measurement of their spectral absorption.

(S. Vézina and W.F. Vincent, unpublished data).

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Mat-forming cyanobacteria – biodiversityPolar microbial mats contain diverse taxa of Bacteria, Archaea, Eukaryotes and viruses (mostly bacterial phages). Metagenomic analyses of mats growing in ice shelf meltpools in the Arctic and Antarctica have revealed that Proteobacteria are the main bacterial phyla associated with the cyanobacteria (figure below, modified from Varin et al. 2010; the inset refers to alpha- (A), beta- (B), gamma- (G) and other (O) Proteobacteria). The eukaryotes include metazoans such as nematodes, rotifers and tardigrades, as well as diatoms, green algae, ciliates and other protists.

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Mat-forming cyanobacteria – the cold biosphere16S rRNA gene comparisons show that many of the High Arctic oscillatorians cluster with Antarctic and alpine cyanobacteria, including with taxa previously thought to be endemic to Antarctica. These pole-to-pole comparisons imply that specialized cold-tolerant ecotypes of cyanobacteria are globally distributed throughout the cold biosphere (figure below modified from Jungblut et al. 2010). More detailed genomic analyses are required to test this hypothesis at multiple alpine and polar locations.

Larsemann & Vestfold Hills, Antarctica

Ellesmere Island, High Arctic, Canada

Tian Shan Mtns, China

McMurdo Ice Shelf & Dry Valleys, Antarctica

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References

 Andersen DT, Sumner DY, Hawes I, Webster-Brown J, McKay CP (2011) Discovery of large conical stromatolites in Lake Untersee, Antarctica. Geobiology 9: 280-293 Hawes I, Schwarz AM (2001) Absorption and utilization of irradiance by cyanobacterial mats in two ice-covered Antarctic lakes with contrasting light climates. J Phycol 37: 5-15Jungblut AD, Lovejoy C, Vincent WF (2010) Global distribution of cyanobacterial ecotypes in the cold biosphere. ISME J 4: 191-202 Leslie A (1879) The Arctic voyages of Adolf Erik Nordenskiöld. MacMillan and Co., London Lovejoy C, Vincent WF, Bonilla S, Roy S, Martineau MJ, Terrado R, Potvin M, Massana R, Pedros-Alio C (2007) Distribution, phylogeny and growth of cold-adapted picoprasinophytes in arctic seas. J Phycol 43: 78-89 Vallières C, Retamal L, Osburn C, Vincent WF (2008) Bacterial production and microbial food web structure in a large arctic river and the coastal Arctic Ocean. J Mar Systems 74: 756-773Tanabe Y, Ohtan S, Kasamatsu N, Fukuchi M, Kudoh S (2010) Photophysiological responses of phytobenthic communities to the strong light and UV in Antarctic shallow lakes. Polar Biol 33:85–100 Varin T, Lovejoy C, Jungblut AD, Vincent WF, Corbeil J (2010) Metagenomic profiling of Arctic microbial mat communities as nutrient scavenging and recycling systems. Limnol Oceanogr 55: 1901–1911Vincent WF (2000) Cyanobacterial dominance in the polar regions. In Whitton BA, Potts.M (eds) Ecology of the Cyanobacteria: their Diversity in Time and Space. Kluwer Academic Publishers, Dordrecht, pp 321-340Vincent WF, 4Quesada A (2012). Cyanobacteria in high latitude lakes, rivers and seas. In: Whitton BA (ed.) Ecology of Cyanobacteria II Springer, DordrechtWharton RA Jr, Parker BC, Simmons GM Jr (1983) Distribution, species composition and morphology of algal mats in Antarctic dry valley lakes. Phycologia 22:355-365

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