Cyanobacterial diversity and dominance
in polar aquatic ecosystems
WARWICK F. VINCENT 1 & ANTONIO QUESADA2
1Centre
for Northern Studies (CEN) & Dépt de Biologie,
Laval University, Québec City, Canada
2 Dpto de Biología, Universidad Autónoma de Madrid,
Madrid, Spain
Online with Ecology of Cyanobacteria II (Chap. 27)
Whitton BA (ed.) (2012) Springer, Dordrecht.
Images (other than those acknowledged)
copyright of authors of article
2
CONTENTS
Introduction
Picocyanobacteria
Mat-forming cyanobacteria
Nostoc communities
Oscillatorian mats
Pigments
Light capture and
photosynthesis
Biodiversity
The cold biosphere
References
3
7
13
14
15
16
19
20
21
22
Supplemental material :
Video 1
Video 2
All images and videos are reproduced with permission; individual
acknowledgements with images
Introduction
Early 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"
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 nitrogenfixing species Calothrix parietina.
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.
5
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).
6
High latitude cyanobacteria
Most of the aquatic taxa fall into three main ecological groups (Vincent
and Quesada 2012):
1) Picocyanobacteria These cells are typically around 1 µm in crosssectional 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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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.
Samples from ice-covered Lake A in the Canadian High Arctic under light (left) and
epifluorescence (right) microscopy.
8
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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Picocyanobacteria in Arctic fjords - 1
Epishelf lakes and fjords
Picocyanobacteria occur in the surface freshwaters of Milne Fjord epishelf lake in the
CanadianMilne
High Arctic,
but are present
only low
concentrations in the underlying seawater.
Fiord
- 13 inJuly
2007
Temperature (°C)
-2,0
0
-1,5
-1,0
-0,5
0,0
0,5
1,0
1,5
2,0
Mid-summer ice – 1.1 m
0.6 ppt
Halocline
at 16 m
Depth (m)
20
Milne Fjord
epishelf lake
40
60
0
5
10
15
20
25
30
35
Salinity (ppt)
D.R. Mueller, Carleton University
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Picocyanobacteria in Arctic fjords - 2
Picocyanobacteria 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.
Picocyanobacteria
(cells ml-1)
cellules.ml-1
0.0E+00
1
5.0E+05
1.0E+06
1.5E+06
ICE COVER
6
Analysis by flow cytometry
of the communities in Lake
A (above) and the counts
for Milne Fjord. Marie
Lionard, unpublished data,
CEN, Université Laval.
Depth
(m)
Profondeur(m)
8
10
12
Temperature =
+1.3oC
picocyano
14
16
18
22
30
Temperature =
-1.4oC
Picocyanobacteria in rivers
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Picocyanobacteria 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).
Picocyanobacteria in the Arctic Ocean
Picocyanobacterial 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).
12
13
Cyanobacteria 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.
Mat-forming cyanobacteria
Mat-forming cyanobacteria - Nostoc
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Mats 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 - Oscillatorians
Many 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- & phycocyaninrich bottom layer where
most of the photosynthesis
is localised.
Mat-forming cyanobacteria -pigments
16
These 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)
17
Oscillatorian 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.
Mat-forming cyanobacteria -pigments
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).
Mat-forming cyanobacteria pigments
The 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 photosynthesis
19
The 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).
Mat-forming cyanobacteria – biodiversity
20
Polar 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.
% of Proteobacteria
Precent of total gene sequences
100
10
100
10
1
A
B
G
O
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0.01
Eu
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Viral
Diversity
Mat-forming cyanobacteria – the cold biosphere
21
16S 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.
Ellesmere Island, High Arctic, Canada
Tian Shan Mtns, China
Larsemann & Vestfold Hills,
Antarctica
McMurdo Ice Shelf & Dry
Valleys, Antarctica
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: 5-15
Jungblut 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: 756-773
Tanabe 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: 1901–1911
Vincent 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 321-340
Vincent WF, 4Quesada A (2012). Cyanobacteria in high latitude lakes, rivers and seas. In:
Whitton BA (ed.) Ecology of Cyanobacteria II Springer, Dordrecht
Wharton 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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