Characteristics of Arctic microbial mats - Mémoire présenté à la Faculté des études supérieures

Taronontic composition

Cyanobacteria were the dominant component of the arctic microbial mats from Ward Hunt Lake and the Resolute ponds and lakes, as elsewhere in the polar zones (Vincent 2000).

blany other studies on periphyton from ponds, streams and lakes have similarly observed that cyanobactena are dominant or CO-dominant with the chlorophytes andlor diatoms of the benthic flora in the Arctic (Stanley 1976, Sheath & Cole 1992, Sheath & Miiller 1997. Vézina & Vincent 1997, Quesada et al. 1999) and dso in Antarctica (Broady 1982, 1989, Vincent 1988, Vincent et al. 1993bl 1993~). The success and dominance of high-latitude cyanobacteria are the result of their high tolerance to stress within the polar environment associated with desiccation, freezing and extreme low temperature (Vincent 2000). The production of the mucopolysaccharide maük (Vincent 1988, Stal 1995) and other anti-fieeze compounds (Tearle 1957, in Davey 1989) confer a protection against these stresses. Cyanobacteria are not adapted to cold temperature but are able to survive and grow at low temperatmes: which are often well below their optimum for maximal gowth (Tang & Vincent 1999). Thus, among the three niche strategies adopted by the organisms living in the cold regions (see Vincent & Quesada 1997). the cyanobactena are eurythermal species and are generalists d e r than specialized genotypes.

Only two cyanobacteria species found in the microbial mats at Ward Hunt Lake have been observed in the benthic communities elsewhere in the arctic region. Nostoc commune, the biovolume dominant in this study, is common throughout the Arctic (Croasdaie 1973, Sheath &

Cole 1992, Sheath et al. 1996, Sheath & Müller 1997, Vézina & Vincent 1997), and Calothrix parietina was found in Greenland (Vincent 2000). There were also some similarities with the microbial mat flora from Antarctica such the presence of Caloihrk parietina (Broady 1982), Nostoc commune (Vincent & Howard-Williams 1986, Vincent et al. 1993b, 1993c) and oscillatonans (Broady 1982, Vincent et al. 1993b). However, the flora diffes markedly in some aspects Eom the ice shelf in the Ross Sea region, Antarctica, by the fkequency of chroococcoid cyanobacteria (P. Broady, pers. corn.). The community also m e n fiom that on the nearby

Ward Hunt Ice Shelf in which the rnicrobial mats are dominated by oscillatorians and chlorophytes, but with no Nostoc, Calothrik or Cymbella spp. (Vincent er al. 2000).

The species Nostoc commune appears to be a characteristic taxon of benthic communities in the non-marine polar environment. Nostoc spp. are widespread throughout in the world (Dodds et al. 1995) and can be an important source of fixed nitrogen for the lakes, ponds and streams in

the polar environment (..Ue?rander et al. 1989. Hawes et al. 1993). h o n g many feanires that are likely to favour the success of this genus in the cold regions are: the high tolerance to desiccation (Hawes er al. 1992), an ability to withstand freezing (Becker 1982), the avoidance of W exposure by production of screening compounds (e.g.. scponemin; Vincent & Quesada 1997), protection against reactive oxygen species induced by UV (Vincent & Roy 1993, and nitlogen fisation and photosythesis at low temperame (OaC) (Lennihan et al. 1994). These adaptations are not limited to iVosroc spp. and are shared with many other cyanobactrrial species, but is it the combination of these characteristics that has to led the enormous success of this genus (Dodds et al. 1995). This genuç appem to be hi-&y tolerant of extreme conditions in the k c t i c (Lennihan et al. 1994) and its presence was therefore to be expected at Ward Hunt Lake. Some of the adaptations mentioned (swival of keeze-up and

Nc

fixation and photosythesis ar O°C) could possibly allow Nostoc spp. to continue a metabolic activity during the period of ice formation in the shallows of Ward Hunt Lake at the end of the summer and dso at the springthe. and thus prolong its growth season. The dominance of Nostoc commzine in our samples couid also be associated with the presence of carbonate rocks at this site; cyanobactena such as

vost toc

commune are often conspicuous in calcareous regions (Whitton 1992). This genus is often favoured in periodically eqosed environments such as ep hemeral fieshwter habitats (Vincent 1988, Hawes & Brazier 1991). This does not appear to be a factor in the continuously submerged environments that we sarnpled in the present study, although at longer timescales (e.g., decades) variations in lake level may select for organisms with this attribute.

The diatom composition withlli the mats represents a srpicd nordic flora. Achnanthes minutissima, C p b e l l a affinis, C. angtrstata and C. cesatii have been previously found in Arctic Canada (Moore 1 9 79, Sheath & Co le 1 992); Achnanthes flexella and Naviala p e m inuta have been reported fiom Siberia (Lange-Bertalot & Genkal 1999); five of the remaining species are

known fkom nordic alpine or mountainous areas in Europe: Achanthes flexella,

C'belZa

cf.

afznis, C. angustata, C. arctica, C. delicatula (Krammer & Lange-Bertaiot 1986, 199 1, Hustedt 196 1-1966). None of the species found in the present study has been reported fiom benthic aquatic communities in htarctica, suggesting fiuidamentai biogeographical difference between the two polar regions. The cosmopolitan species Achnanrhes mintltissima had the highest biovolume within the diatom groups. This species c m live in a wide environmental range of conditions including hotsprings Nilleneuve & Pienitz 1998) and qpears to grow abundantly in the more temperate regions of North America (Moore 1979). Another notable charactenstic of the diatom assemblage is the relatively high number of Cymbella species ( 6 ) in the microbial mats, dorninated by Cymbella cf. afinis, C. angustatu and C . delicarula. This observation has not been previously made for microbial mats in the polar environment.

The chlorophytes conbibuted a hi& total biovolume at fluvial site El (15.3 %) by cornparison with the sires E2 (0.6 %) and E3 (0.8 %). Codominance of chlorophytes and cyanophytes has offen been reported in the periphyton from streams in the Arctic (Sheath & Cole 1992, Sheath et al. 1996, Sheath & Müller 1997) and in Antarctica (Vincent & Howard-Williams 1986, Hawes 1989). The dominant chlorophytes belonpd to the filamentous genera ibhugeotia and Zygnema, as found in Antarctic streams (Hawes 1989) and other .Arctic freshwaters (Sheath er al. 1996, Sheath & Müller 1997). In the fluvial environment, slou-&hg couid be the most important loss process for benthic algae. ï h i s would favour groups which can rapidly attain high cover at Low temperature such as the filamentous chlorophytes (Hawes 1989). Unlike the microbial mats, however, these cornmunities do not accumulate biomass, but die back at the end of summer and have to recolonize the environment at the beginning of each growing season (Hawes 1989, Vincent et al. 1993~).

The biodiversity of the microbial mats _{fiom Ward}Hunt Lake (49 taxa), seems particularly hi& given the extleme climatic conditions at this northern latitude. The number of taxa is dso high for a single waterbody relative to other studies fiom the Arctic and Antarctica, where higher numbers of benthic taxa have been obtatied but, by sampling numerous study sites (Table 1.14).

The total number of taxa reported by Vézina & Vincent (1997) for many lakes and ponds at another site in the High Arctic was much lower (37) relative to Ward

Hunt

Lake.

Table 1.14. Benthic algal biodiversity (number of taxa) in streams (S), ponds

(P)

and lakes

CL)

t depending on the type of substrate sampled (rocks, sedimens, sana higher plants)

included three reaches of a strearn (upper, middle and lower) and a pond

9 numerous ponds and streams were sampled at three sites

Pigrnenfi

The total Ch1 a and carotenoid content of microbial mats at Ward Hunt Lake and Resolute lakes are generally within the range for mats in the Arctic (Vézha & Vincent 1997, Quesada et a!. 1999) and Antarctica (Vincent et al. 1993b), although concentrations can be much lower at some polar sites (Hawes et al. 1993). The carotenoid to Ch1 a ratio in this study was higher relative to other studies which generally obtained ratios Iower than 1 .O. Differences in the method of extractim could be a factor evplaining this difference relative to Vézina & Vincent (1 997) and Vincent et al. (1993b), but this would not be the case with the midy by Quesada et al. (1999) who applied a similar method to the present study with repeated extractions.

Ch emical ch aracterktics

The high concentrations of nuh-ients and major ions within the mats are may be caused by the accumulation of these compounds as a result of bioeeochemical processes. although Freeze concentration may also be a factor (see below). The combination of high respiration rates in cornparison to the photosynthetic activity could be one factor leading to the high DIC concentrations observed within the mats. Respiration in cyanobacterial mats can account for 90

% or more of gross photosynthesis (Vincent & Howard-Williams 1989). Aise' the self-shading by the algae may lirnit their growth (Hansson 1992, Hawes et al. 1993), and thus their photosynthetic uptake of carbon. The absence a light-dark cycle during summer in the polar zones should allow a continuous photosynthesis by the mat algae but would not seem to be sufficient to deplete the in situ concentrations of DIC. Heterotrophic bactena within the mats may aiso contribute to the

DIC

pool by the respiration of the photospthetic exudates ( D o m e s et al.

1986, in Wym-Williams 1990). Other heterotrophs such as protozoa rnay similarly contribute to DIC by respiration, although this input is iikely to be small.

w e a t h e ~ g of the carbonated rocks by carbonic acid may provide a large supply of inorganic carbon as bicarbonate (HCO37 which remains in solution in the interstitial m t e r of the mats because of a reversible reaction between the calcium and bicarbonate ( ~ a " + 2HC03' * Ca(HC03)2). Calcium and inorganic carbon can be precipitated out as CaC03 by photoqmthetic CO2 uptake (Hawes & Schwarz 1999). However, given the hi& respiration rate, CO2 depletion leading to carbonate precipitation seems iiniikely.

High concentrations of inorganic nitrogen and phosphorus were also measured in the microbiai mats from Antarctica with two orders of magnitude higher

SRP

in the mats relative to the overlying water (Vincent et al. ^1993a).Hi& concentrations of

w'-N

were found in the present snidy and seem musual because of the adequate oxygen conditions within the mats for nitrification. The absence of nitritehitrate in the mats suggests an inhibition of nitrification processes or, dtemrtivdy, a r i g k cc1inlinn UPd'AAE between pmduction and lors (Vincesent er ol.

1993a). The dominant species ? h t o c commune is an Nz-fixer and is usually found under conditions of low combined inorganic nitrogen (NK2'-N plus N02/NO;). However. the pool of

m-N

^within^the^matsmay not be available to al1 algae in the mat, and slow molecular difision rnay limit its transport to sites of biological utilization. This difision limitation of available combined-nitrogen could explain the predominance of heterocystous cyanobacteria in the microbial benthic community.

The particdate (POC) and dissolved organic matter (DOC) widiin the mats is mostly fiom the phototrophic organisms. their subsequent death and lysis, and the excretion of exnacellular polymeric substances (e.g., polysaccharides; Stal 1995). Our studies on mats on the adjacent Ward Hunt Ice Shelf have revealed hi& concentrations of Wuses (Vincent et al. 2000): and viral lysis of the cyanobactena and other mat constituents rnay M e r contribute to the hi& DOC

content of the mats via the "viral shunt" (Wilhelm & Suttle 1999). Sedimentation of phytoplankronic cells fiom the overlying lakewater may also contribute to POC and DOC within the mats, but this input is probably minor given the low phytoplanktonic biomass. The high concentration of dissolved organic nitrogen

@ON)

and the organic fiachon of

TDP

also reflecü the accumulation of biological products fkom algal death and lysis, as weli as excretion by Living cells. Little of this organic material is likeIy to corne fIom allochthonous sources outside the lake.

The concentration of CDOM, the coloured dissolved organic matter fkom vegetation and soils in the catchment, was found to be extremely low in the lakewater (Gibson et al. submitted).

The hi& concentrations of nutrients within the mat interstitial water is unlikely to be a major source of nutrients for the lakewater because of the slow rnolecular diffusion rate across the mat boundary layer. As pointed out by Pearl et al. (1993), the stlategy adopted by microbiai

mats appears to optimize nutrient inputs and minimize losses to ensure optimal rates of production and biomass accumulation.

Freeze-concentration is likely to be the main process explaining the hi& concentration of major ions in the interstitial water of the mats, and is also likely to have contributed to the hi&

nutrient concentrations. Studies in shallow Antarctic lakes and ponds have s h o m that ions are exdnded h m the ice d ~ r g t'l- freeze-np of the overlyhg water and t h c m to

increases in salinity, up to five t h e s that of seawater, within the remaining liquid water (Schmidt et al. 1991). The on* of these ions in the Ward Hunt mats rnay be mainiy fiom the marine aerosols because of the proximity to the sea. The ionic concentrations in the surface lakewater (SL) are low because of the fast water renewai, while freeze-concentration is likely to be a long t e m process. Other biogeochemical processes may operate on the ionic ratios that we measured in the mats and thereby cause departures from the ratios found in sea wvater. N a and Cl- are the a higher ca2- and big2+ content because of the higher concentration of the former in the mats.

High concentrations of silica in the Ward

Hunt

mats have not been mentioned in previous snidies of polar microbial mats. The elevated values found here may be the result of silica dissolution (as silicic acid, H2Si04) fiom diatom M e s accumdated in the mats. The concentration of SiOz are one order of magnitude higher relative to the concentration in seawater, whereas the absolute concentration of the other major ions in the mats are well below concentrations found in seawater, by 2 to 4 orders of magnitude. Bacterial activiv within the mats could be a source of suiphate and thereby explain the high concentrations of SO~". The degradation of organic matter in the microbial mats is likely to generate d p h i d e (H2S) which can be subsequently oxidized to sulphate by colorless and purple mlphur bactena (van Gemerden 1993). Sulphate reduction can also occur in the presence of oxygen (van Gemerden 1993) and mi@ therefore operate in the oxygenated mats we obsemed at Ward

Hunt.

High concentrations of major ions within the mats suggest an ability of the organisms to withstand a high osmotic stress (Schmidt et al. 199 1). This may be one of several determinants of sunival in the harsh polar environment associated with fieeze-up and desiccahon (Vincent 1988).

Spatial variations Vertim! s ~ a r i f cnt io n

A pronounced vertical stratification of the Chi a and carotenoid pigment concentrations vas observed within the mats, with an upper orange layer overlaying the Lower blue-green straturn. The high concentration of carotenoids within the upper layer probably masked the green pigment Ch1 a. The lower blue-green coloration is likely to be the result of Chl a in combination with hi& concentntion of phycocyanin (Vincent et al. 1993 b), the PSI1 accessory pi-ment that is characteristic of cyanobacteria. Highest concentrations of Ch1 a and carotenoids (in absolute values) occurred in the upper mat sections. This contrasts with several other studies that measured higher concentrations at the bottom (Vincent et al. 1993b. Howard-Williams & Vincent 1989 (Ch1 a only), Quesada ef al. 1999). Carotenoid pigments play a role in protecting cells against the harmfui effects of ultraviolet radiation, such the formation of hi+dhly reactive oxygen species (e.g., hydrogen peroxide, superoxide radicals; Vincent & Quesada 1994, Vincent 8r Roy 1993). Its presence in hi& concentration in the upper layers would therefore confer protection to the rest of the mat comrnunity. The lower strata of the mats did not show elevated oxygen tensions (and much less L&t) and therefore there would be a lesser need for anti-oxidants such as the carotenoids karotene and echinenone (Vincent et al. 1993b). We found some cells in the mats to be pdcularly rich in carotenoids. These were in the category "unidentified" (Table 1.2) but resembled chiorophyte spores fiom the snow algae Chlamydomonas nivalis. These spores are known to accumulate lipid globules and secondary carotenoids that likely to play the same photoprotective role in high albedo snow and ice environments (Bidigare et al. 1993). The bulk of autotrophic activity seerns to be resûicted to the upper strata in these mats, where the relative proportion of Ch1 a pigments is higher relative to the bonom. We did not observe a "deep Ch1 a maximum" as reported in Antarctic mats (Vincent et al. 1993a), however the lower layer was rich in light-capturing phycobih and autotrophic activity is likely to be substantial in this lower matum. A portion of the Chl a rnay be inactive pigments preserved within the mats after cellular

death (Howard-Williams et al. 1989a). However, our biovolume data show the presence of intact algae in both strata and indicate that Live cells are distributed throughout the mat profile.

The greeater total biovolume in the upper layer of the mats is M e r evidence that the Ward Hunt assemblages are vertically stratified. However, the variable CM a to biovolume ratios could suggest the vertical migration of algae within the mat profiles. Oscillatonan filaments and di~tcns hme the capacity to vertical n@ite in respmre to irradiance (Vincent et nl I W a , Sundback et al. 1996). The Chl a to biovolume ratios did not decrease substantially benveen the uppermost and the lower strata in tandem with irradiance. This is contrary to what might be expected on the basis of previous ecophysiologicai results. For example. Vézina & Vincent (1997) found an order of magnitude increase in the Ch1 a content to biovolume with decreasing irradiance. h additional explmation for the lack of change in the Ch1 ahiovoiume is that the lower layer is likely to contain a greater proportion of inactive Ch1 a associated with the gradud thickening and accumulation of pigment in the mat over tirne. This effect could obscure any physiological differences between the upper and lower saata.

The different taxonomie groups showed no marked differentiation between the upper and lower strata in tems of relative biovolume but instead were distributed hornogeneously throughout the mat profiles. We observed many thin (< 5 pm) fihmentous species such as Phormidium tenue, cf. Pseudoanabaena sp. and Schizothrir calcicoia. These species did not make a large contribution to total biovolume. for example by cornparison with the spherical colonies of Nostoc commune (45 prn dia in mean). However, these organisms may be disproportionately important contributors to primary production within the mats because they have minimal self-shading and an excellent light-capturing efficiency, and are highly advantaged under low light conditions (Vincent 2000), which characterize the lower layers of the mats.

Mucilage production by these species may also be a major contributor to the total organic carbon content as well as cohesiveness of the mats.

The pH and oxygen profiles showed no evidence of an increase in photosynthesis with depth, but instead implied a shift towards a negative photosynthet.Ïc/respiratory balance down the mat profiles. Contrary to some rnicrobial mat systems studied in the polar zone (Ellis-Evans &

Bayliss 1993, Vincent et al. 1993a), no anoxic zone was observed at the bottom of the mats, excepted for profile E l b (Fig. 1.17). The thickness of the Arctic mats (mau. 5 mm) relative to the thick mats studied in the Antarctica (e.g., 20 mm; Vincent et al. 1993a), may be a factor

responsible for this difference. Different processes in mats control the oxygen budget over the coune of the day and the night and this die1 variability appears to be important in microbial mats of the temperate zone (Canfield & Des Marais 1994). Polar microbial mats offer an interesthg conm liecause of the continuous light availability for photosynthesis. conditions that might be expected to result in O2 supersaturation. Even if the absolute saturation values are hi& at low temperature, it remains that the Oz concentrations obtained here are only at a ma.uimum of 30%

of the saturation value. The photosynthetic rates are likely to be very low in the Arctic mats and the respiration a high part of the goss photosynthesis which would tend to reduce the accumulation of oxygen (Vincent & Howard-Williams 1986).

Microhetero~ophs such as bacteria and protozoa are known to be an integral part of the microbial mat communities from htarctica (Vincent 1988). Different -pes of bacteria with specific roles live 1vith.h microbial mats at different depths depending on Oz and light availability (e.g., van Gemerden 1993, Paerl & Pinckney 1996). Such bacteria couid play an important role in the nutrient cycling and may also influence the gr01wt.h of cyanobactena through ailelopathic and

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