Cyanobacteria are gram-negative, oxygenic phototrophic bacteria that evolved more than 2.5 billion years ago. They use blue or red coloured proteins (phycobiliproteins) in addition to chlorophyll a and can be found in aquatic, terrestrial and marine environments worldwide. They are especially successful in extreme habitats, such as the permanently cold environments of the Polar regions due their striking array of adaptations to withstand the extreme conditions of permanently cold environments.
Especially aquatic, benthic cyanobacteria can accumulate very high biomass, from mm to cm thick cyanobacterial mats. They can often cover the entire bottom of shallow terrestrial freshwater ponds and ice shelf meltwater ponds, where grazers, which are common in temperate and tropical environments, are lacking in many polar environments. Stringent conditions of the Arctic restrict the growth of aquatic plants, macrophytes and bryophytes in Arctic lakes and ponds, and cyanobacteria are often crucial contributor to primary production and key elements of Arctic benthic freshwater food webs. This also includes glacial habitats such as cryoconite holes.
Cyanobacteria are also widespread in terrestrial soil environments, where they are important primary producers in rock-associated microbial habitats, provide stability to the soils as soil crusts, and contribute to terrestrial nutrient cycling as endosymbiotic nitrogen-fixing cyanobacteria in lichens.
Arctic cyanobacteria diversity
Cyanobacteria are microscopic but because they often form macroscopic biofilms, crusts and mats, they can be visible with the bare eyes, and therefore it is not surprising that they were already described early in the exploration of the Arctic. For example, Erik Nordenskiöld reported the presence of dark particulate material on the ice, which became known as cryoconites from his expedition to the Greenland ice sheet in 1870 (Maurette et al. 1986). A Swedish expedition to Svalbard noted the presence of the cyanobacterium Nostoc from fellfield pools in Spitsbergen in 1861 (Leslie 1879). Since then many different cyanobacteria have been reported from Arctic terrestrial environments using morphological descriptions, environmental DNA sequencing and enrichment isolation techniques.
Cyanobacteria belonging to the orders Oscillatoriales (filamentous without heterocyst-forming, non-branching), Nostocales (filamentous, non-branching heterocyst-forming) and unicellular cyanobacteria (Chroococcales) are the most commonly reported taxa in terrestrial and benthic freshwater environments of the Arctic. In freshwater lakes, ponds, streams and glacial cryoconites, the benthic cyanobacterial assemblages are usually dominated by oscillatorian genera such as Oscillatoria, Phormidium, Pseudanabaena, Microcoleus, and Leptolynbya (Jungblut et al. 2012, Kim et al. 2008, Stibal et al. 2006, Villeneuve et al 2001, see also Zakhia et al. 2010). They are important for the formation of biofilms and microbial mats in streams, ponds and lakes (Vincent 2000). The order Nostocales that entails nitrogen-fixing taxa, such as the genera Dichothrix, Calothrix, Tolypothrix, Anabaena and Nostoc are also common, particularly in nitrogen-poor environments (Jungblut et al. 2012; Villeneuve et al 2001, see also Zakhia et al. 2010).
Cyanobacteria can also be photobiont (phytobiont) in lichens where they form endosymbiotic relationships with fungi (mycoboint, usually an ascomycete). Cyanobionts are always nitrogen-fixing cyanobacteria and provide much of the nitrogen needed by the fungi. Nostoc is the most common cyanobacterial photobiont, but Calothrix, Scytonema and Fischerella can also be found (ref?). Other potential advantages of the cyanobiont may be production of UV screening substance (see below). Similarly, nitrogen-fixing cyanobacteria also form associations with both mosses and hornworts (e.g. Adams & Duggan 2008). Cyanobacteria may form symbiotic relationships also with several other organisms, e.g. some plants and even animals (corals, sponges, ascidians) in both terrestrial and aquatic habitats. They usually supply fixed nitrogen and or carbon to their partner.
In contrast unicellular cyanobacteria (Chroococcales) are less common in microbial mats but often described from Arctic soils and lithic environments such as below rocks and cracks of rocks (xxx see blow). Descriptions include Gloeocapsa, Chroococcus, Chloroglea, Aphanocapsa, Gomphosphaeria, Aphanothece, Chroococcidiopsis, Merismopedia and Synechoccus (Jungblut et al. 2012; Villeneuve et al 2001, see also Zakhia et al. 2010).
Biogeographical distribution and dispersal
Cyanobacteria isolated from cold environments have nearly all temperature optima growth rates in the range of 15–20 °C, suggesting that they likely had their evolutionary origins within temperate latitudes (Tang et al. 1997, Nadeau et al. 2001) and subsequently colonized perennial cold habitats. Furthermore, molecular clock analysis suggested that cyanobacteria from hot and cold desert have diverged a long time ago from ?cold cyanobacteria in cold habitats? (Pointing et al 2009). Antarctic cyanobacteria may have survived Antarctic glaciations in refugia to green algae and microfauna (after the break-up of Godwana (Stucnkey 2012, DeWever et al. 2009) and a similar process can be expected to have happened in the Arctic.
Although cyanobacteria are widely distributed in the Arctic, and there are numerous studies on cyanobacterial diversity, the biogeographic distribution of cyanobacteria is still a topic of much discussion.
Studies of Arctic and Antarctic oscillatorians based on morphological and molecular methods have reported endemic as well as cosmopolitan taxa (Comte et al. 2007, Jungblut et al. 2010). For example ITS-regions of Phormidium autumnale Arctic strains from Svalbard and Antarctica were so different that they might be endemic (Comte et al. 2007). As an opposing example, oscillatorian cyanobacteria from high Arctic benthic freshwater mats had some species with ribotypes that were >99% similar to Antarctic and alpine sequences, but dissimilar to sequences from other climatic zones. This would imply a global distribution of low-temperature cyanobacterial ecotypes throughout the cold terrestrial biosphere (Jungblut et al. 2010).
This raises the question of the dispersal mechanisms for cyanobacteria within the Arctic. It seems that they can be transported – at least over local distances – by air (e.g. Harding et al. 2012, Møller et al. xxxx, Pearce et al. 2009). Although theoretical transport of particulars is possible from the Southern to the Northern Hemisphere (Griffin et al. 2002), there is still a lack of evidence that proves the atmospheric dispersal of cyanobacterial from pole to pole. Only few cyanobacteria were found in aerosol, snow and ice samples from remote glaciers from Antarctic, Alpes and Andes, and none of those seemed to be viable (Elster et al. 2007).
How do cyanobacteria cope with the Arctic conditions?
In the Arctic, cyanobacteria are exposed to a variety of environmental stresses in both terrestrial and aquatic ecosystems. They have several adaptations, which help them to grow in the often adverse conditions.
Many cyanobacterial environments completely freeze over the winter, and cyanobacteria have a variety of mechanisms that allows them to tolerate and continue to grow in the cold, albeit often at slow rates (Vincent 2007). Research suggests that benthic freshwater cyanobacteria from Polar Regions tend to be cold tolerant (psychrotrophs), with suboptimal growth under low temperatures, rather than psychrophiles, that grow optimally at low temperature (Tang et al. 1999). This is thought to allow Cyanobacteria to cope better with rapid dial temperature changes in often shallow benthic freshwater environments, such as ice meltwater ponds, terrestrial ponds, and lake shores. However, it is not known if this is also the same case for planktonic cyanobacteria found in Arctic freshwater ecosystems that are often unicellular picocyanobacteria (Van Hove et al 2008).
Although there is a limited number of studies on Arctic cyanobacteria, we have some understanding of adaptation mechanisms based on physiological laboratory and Antarctic field studies. For example, it has been shown that cyanobacteria can maintain membrane fluidity at low temperature by incorporation of polyunsaturated fatty acids with decreased chain-lengths into the cell wall membranes (Laybourn-Parry 2002, Suzuki 2001).
High UV radiation can be also a major stress for cyanobacteria in the Arctic, because UV radiation and high energy PAR can induce photo-inhibition, phycobiliprotein degradation, chlorophyll-bleaching, DNA damage and generate reactive oxygen species (Castenholz 1992, Ehling-Schulz and Scherer 1999). Cyanobacteria have evolved a variety of DNA repair mechanisms, such as excision repair and photo-reactivation, to cope with UV induced DNA damage (Garcia-Pichel and Castenholz 1991, and review by Castenholz & Gacia-Pichel 2012).
A striking feature of Arctic benthic cyanobacterial communities is their richness and diversity of pigments to overcome high PAR and UV radiation stress. A comparison of mat communities across northern Canada and Alaska showed that photoprotective pigments increased with increasing latitude, decreasing water temperature and increased UVR transparency of the overlying water (Bonilla et al. 2009). This includes in particular the production of photoprotective screening and quenching pigments, such as gloeocapsin, mycosporine and scytonemin, which absorb UV-A and UV-B radiation, and carotenoids acting as anti-oxidants. High concentrations of the UV-screening compound scytonemin can lead to a black coloration in many cyanobacterial mats and soil crusts (Vincent and Quesada 1994). Motile osccillatorian cyanobacteria inside benthic mats may move deeper down into the mats as well, to reduce exposure to the UV radiation (Quesada & Vincent 1997, Antarctica).