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Extremotrophs, Extremophiles and Broadband Pigmentation Strategies in a High Arctic Ice Shelf Ecosystem

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Extremotrophs, Extremophiles and Broadband Pigmentation Strategies in a High Arctic Ice Shelf Ecosystem FEMS Microbiology Ecology 53 (2005) 73–87 www.fems-microbiology.org Extremotrophs, extremophiles and broadband pigmentation strategies in a high arctic ice shelf ecosystem Derek R. Mueller a,*, Warwick F. Vincent a, Sylvia Bonilla a,b, Isabelle Laurion c a Centre dÕe´tudes nordiques et De´partement de biologie, Universite´ Laval, Pavillon Vachon, Quebec City, QC, Canada G1K 7P4 b Facultad de Ciencias, Universidad de la Repu´blica, Montevideo, Uruguay c Institut national de la recherche scientifique, Centre Eau, Terre et Environnement, Quebec City QC, Canada Received 30 June 2004; received in revised form 5 November 2004; accepted 5 November 2004 First published online 23 November 2004 Abstract Remnant ice shelves along the northern coast of Ellesmere Island, Nunavut, Canada (83°N) provide a habitat for cryo-tolerant microbial mat communities. Bioassays of bacterial and primary production were undertaken to quantify the short-term physiolog- ical response of the mats to changes in key variables that characterize this cryo-ecosystem (salinity, irradiance and temperature). The heterotrophic versus autotrophic community responses to these stressors differed markedly. The heterotrophic bacteria were extrem- ophilic and specifically adapted to ambient conditions on the ice shelf, whereas the autotrophic community had broader tolerance ranges and optima outside the ambient range. This latter, extremotrophic response may be partly due to a diverse suite of pigments including oligosaccharide mycosporine-like amino acids, scytonemins, carotenoids, phycobiliproteins and chlorophylls that absorb from the near UV-B to red wavelengths. These pigments provide a comprehensive broadband strategy for coping with the multiple stressors of high irradiance, variable salinity and low temperatures in this extreme cryo-environment. Ó 2004 Federation of European Microbiological Societies. Published by Elsevier B.V. All rights reserved. Keywords: Ice shelf; Microbial mats; Scytonemin; Oligosaccharide mycosporine-like amino acid; Productivity; Extremophile; Extremotroph 1. Introduction Phormidium, Leptolyngbya, Nostoc and Gloeocapsa) but also containing a wide variety of other taxa includ- Microbial phototrophs occur in a wide range of ice- ing viruses, heterotrophic bacteria, green micro-algae bound environments including sea ice, glaciers and snow and diatoms, as well as micro-invertebrates [2,3]. [1]. More recently, another type of cryo-ecosystem has Polar microbial mat communities retain a large over- been discovered in the North Polar Region. Similar to wintering biomass and then grow slowly during the brief their Southern Hemisphere equivalents, arctic ice shelves season of liquid water availability [4]. The micro-organ- provide an extreme habitat for microbiota. Microbial isms on the Ward Hunt Ice Shelf deal with a combina- mats constitute the dominant biomass on the Ward tion of physiological stresses imposed by their ambient Hunt Ice Shelf, High Arctic Canada (latitude 83°040N, environment, including cold temperatures (<5 °C), high longitude 74°250W). These are a complex microbial con- levels of solar radiation (including ultraviolet radiation) sortia dominated by cyanobacteria (notably the genera and 10-fold variations in salinity. The conjunction of these conditions makes arctic ice shelves an extreme ha- * bitat type, however the physiological optima and toler- Corresponding author. Tel.: +418 656 2131x8153; fax: +418 656 2043. ance ranges of Ôice-matÕ communities in relation to E-mail address: [email protected] (D.R. Mueller). these stressors have not been quantified. 0168-6496/$22.00 Ó 2004 Federation of European Microbiological Societies. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.femsec.2004.11.001 74 D.R. Mueller et al. / FEMS Microbiology Ecology 53 (2005) 73–87 Many polar microbial mat cyanobacteria are cold- meltwater lakes (up to 15 km long, 3 m deep and tolerant (psychrotrophic) rather than cold-adapted (psy- 10–20 m wide), which run parallel to the Ellesmere Is- chrophilic) with their thermal optima for photosynthesis land coastline (Fig. 1). and growth lying well above their ambient range [5,6]. The distribution of microbial mats across the ice shelf By extension, polar phototrophs may respond to several is highly variable. Typically, microbial mats occur in aspects of their habitats in the same way, with tolerance conjunction with sparse sediment deposits either on to extremes in various environmental dimensions the ice surface or in discrete depressions in the ice sur- (extremotrophs) rather than adaptation towards opti- face termed cryoconite holes (approximately 7% cover; mal growth at or near the extreme conditions experi- D.R. Mueller, unpublished data). In certain areas, enced in situ (extremophiles). Microbial mats where sediment has been concentrated over time [12] elsewhere are known to reduce the effects of high ultra- microbial mats appear to be more developed and are rel- violet (UV) radiation with photo-protectants that atively abundant (18–31% cover over scales of hundreds quench free radicals or act as screening pigments [7,8]. of metres; D.R. Mueller, unpublished data). Polar microbial mats are simultaneously exposed to high Arctic ice shelf microbial mats are typically composed UV irradiances, high photosynthetically active radiation of small olive-green flakes or ÔmatletsÕ that accumulate (PAR) and low temperatures, leaving them particularly to a thickness of several millimetres to centimetres. In prone to photodamage [9], and suggesting that photo- more developed communities, the surface layer (100– protection may be especially important in these systems. 500 lm) is a conspicuous orange colour [3]. Aside from In this multi-stressor environment, a broadband pig- a surface layer, seen in developed communities and a ment strategy that efficiently reduces photodamage black, anoxic layer, observed in very thick sediments, might also free up resources for osmoregulation, thereby these microbial mats do not appear to be further strati- assisting in salinity, freeze–thaw and desiccation toler- fied as found in many microbial mats [13]. ance, and preventing serious damage when these other Microbial mats from northern ice shelves are sub- stressors inhibit metabolic activity and cellular repair jected to a variety of environmental stressors. Further- mechanisms. more, these stressors vary both temporally and The purpose of this paper is to evaluate the physio- spatially, necessitating physiological acclimation on sev- logical attributes of mats in the Ward Hunt Ice Shelf eral timescales. A pronounced seasonality at this high cryo-ecosystem and to address the question of how these latitude site causes gradual but extreme changes in light consortia respond to physical and chemical stresses in photoperiod (147 days of continuous darkness in winter their high arctic environment. These communities occur and 147 days of continuous light in summer) and irradi- today in the Arctic and Antarctica, but may have been ance (0–1200 lmol photons mÀ2 sÀ1 downwelling PAR), more widespread during periods of extreme cooling in temperature (average mat temperature = À8.6 °C, max- the past [10]. We first quantified the primary production imum = 1.7 °C, minimum = À15.7 °C; D.R. Mueller, and bacterial heterotrophic production of northern ice unpublished data from automated in situ dataloggers) shelf microbial mat consortia under representative and the availability of liquid water. mid-melt season conditions. We then addressed the During the summer months, the ice shelf environment hypothesis that these mats subsist in sub-optimal condi- is more dynamic due to temperature shifts across the tions by determining their metabolic response to short- freezing point of water. Microbial mats emerge sporad- term changes in light regime, temperature, salinity and ically from under melting snow and ice over the course hydration. We identified and quantified pigments of the summer months resulting in a 10-fold increase (including UV absorbing compounds, some of which in light levels. Periods of high irradiances due to low so- may be transparent in the PAR waveband) in these microbial mats, specifically chlorophylls, carotenoids, scytonemins and mycosporine-like amino acids (MAAs), to determine to what extent the potential for photoprotection exists within these communities. 2. Methods 2.1. Study site The Ward Hunt Ice Shelf is a 40 m thick free-float- ing mass of ice that accreted in situ over the last 4500 years [11]. The surface of the ice shelf is marked by a ridge and trough morphology that is associated with Fig. 1. Location of ice shelves in Nunavut, Canada. D.R. Mueller et al. / FEMS Microbiology Ecology 53 (2005) 73–87 75 lar angles and reflection from high albedo surfaces such ing sphere. The filters did not affect the spectral as snow and ice are punctuated by periods of intense fog distribution of light between 400 and 700 nm. The treat- in which ambient irradiances are much reduced. In ments reduced PAR levels to 0 (dark), 1%, 6%, 10% and spring, meltwater influx reduces the salinity of water 22%, 45% and 82% of ambient light. UV-A (320–400 that overlies the microbial mats, with conductivities nm) levels were 5%, 8%, 11%, 17%, 35% and 80% of ranging from fresh (0.5 mS cmÀ1) during periods of ambient and UV-B (300–320 nm, in this case) levels were open water to saline (>10 mS cmÀ1) during freeze-up. 26%, 28%, 34%, 36%, 42% and 85% of ambient light. During summer, in the absence of turbulent mixing, Samples were placed outside
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