Effect of temperature on the growth rates of halotolerant and halophilic bacteria isolated from Antarctic saline lakes

Summary The effect of temperature on the growth rates of Halomonas subglaciescola and a Halobacterium sp., halotolerant and halophilic bacteria isolated from Antarctic saline lakes, was predicted accurately by models which propose a linear relationship between temperature and the square root of the reciprocal of the growth rate. The cardinal temperatures of the strains examined were in general 5–10°C lower than those of taxonomic counterparts isolated from temperate and tropical environments. Temperature dependence data for strains of the Halobacterium sp. and annual temperature profiles of Deep Lake allowed estimation of the in situ potential for growth.     

Survival mechanisms in Antarctic lakes

In Antarctic lakes, organisms are confronted by continuous low temperatures as well as a poor light climate and nutrient limitation. Such extreme environments support truncated food webs with no fish, few metazoans and a dominance of microbial plankton. The key to success lies in entering the short Antarctic summer with actively growing populations. In many cases, the most successful organisms continue to function throughout the year. The few crustacean zooplankton remain active in the winter months, surviving on endogenous energy reserves and, in some cases, continuing development. Among the Protozoa, mixotrophy is an important nutritional strategy. In the extreme lakes of the McMurdo Dry Valleys, planktonic cryptophytes are forced to sustain a mixotrophic strategy and cannot survive by photosynthesis alone. The dependence on ingesting bacteria varies seasonally and with depth in the water column. In the Vestfold Hills, Pyramimonas, which dominates the plankton of some of the saline lakes, also resorts to mixotrophy, but does become entirely photosynthetic at mid-summer. Mixotrophic ciliates are also common and the entirely photosynthetic ciliate Mesodinium rubrum has a widespread distribution in the saline lakes of the Vestfold Hills, where it attains high concentrations. Bacteria continue to grow all year, showing cycles that appear to be related to the availability of dissolved organic carbon. In saline lakes, bacteria experience sub-zero temperatures for long periods of the year and have developed biochemical adaptations that include anti-freeze proteins, changes in the concentrations of polyunsaturated fatty acids in their membranes and suites of low-temperature enzymes.     

Ecologic Aspects of Protozoan Infections in Antarctic Fishes1

ABSTRACT. Plankton and fishes are abundant in Antarctic waters. Benthic invertebrates and fishes of the continental shelf are well-known, but the abyssal benthos below the highly productive open ocean is largely unsampled. The fishes are adapted (with antifreeze properties) to temperatures that are often or always below the freezing points of their body fluids. All the major groups of helminth parasites are found in or on these fishes. The few records of protozoa include Cryptobia, haemogregarines, a monoflagellate, the myxosporan Neoparvicapsula, and (in this paper) Ceratomyxa. Myxidium, Zschokkella, and a coccidian. Most of the protozoa were obtained from nototheniid fishes. No protozoa and few, if any, other parasites were recovered from 173 midwater fishes collected from outside of the continental shelf. Differences in infections in different localities and depths are due to many ecologic factors needing much more study of their relations to parasitism. These factors include temperatures, salinities, densities of fish populations, food and feeding habits, migrations of adult and immature fishes, availability of potential intermediate hosts, and marine “snow.”     

Bacterioplankton production in freshwater Antarctic lakes

1. Bacterioplankton production was measured in the water columns of two ultra‐oligotrophic, freshwater Antarctic lakes (Crooked Lake and Lake Druzhby) during an annual cycle. In both lakes bacterial production, measured by the incorporation of [³H] thymidine, continued in winter and showed a cycle over the year. The range of production was between 0 and 479 ng C L^?1 h^?1 in Crooked Lake and 0–354 ng L^?1 h^?1 in Lake Druzhby. 2. Abundance and mean cell volume both varied, producing marked changes in biomass during the year, with highest biomass occurring in the winter and early spring. Biomass showed similar seasonal trends in both lakes. 3. For most of the year inorganic forms of nitrogen and phosphorus were detectable in the water columns of the lakes and were unlikely to have limited bacterial production. Dissolved organic carbon (DOC) was below 3000 μg L^?1. Dissolved amino acids and carbohydrates contributed 5–25% of the DOC pool in Crooked Lake and 5–64% in Lake Druzhby. Dissolved carbohydrates were consistently low, suggesting that this may have been the preferred carbon substrate for bacterioplankton. 4. Aggregate associated bacteria had higher mean cell volume, abundances and production than freely suspended bacteria in Lake Druzhby, while in Crooked Lake aggregate associated bacteria consistently had higher mean cell volumes than free bacteria, but abundance and production were on occasion higher in free bacteria compared with aggregate associated communities. 5. The data indicated that production is limited by continuous low temperatures and the limited availability of suitable DOC substrate. However, the bacterioplankton functions year round, responding to factors other than temperature.     

Methane in maritime Antarctic freshwater lakes

Summary Methane was found to occur in all freshwater lakes, irrespective of trophic status, sampled during this preliminary investigation at Signy Island, South Orkney Islands, Antarctica. Methane accumulated in the water column of these lakes during the winter period when ice cover prevented wind-induced mixing. Maritime Antarctic lakes are usually subject to wind-induced complete mixing during the summer open-water period but two major exceptions to the rule were found during this study. Methanogenesis occurred in both littoral and profundal regions of oligotrophic Sombre Lake. The presence of a substantial algal mat stabilized the Eh status of underlying sediments at the littoral site. Methane production was confined to the sediments in both littoral and profundal sediments during the study period (December–March) but in winter probably migrated to the sediment surface at the profundal site. All Signy Island lakes sampled were sulphate-poor and addition of sulphate markedly inhibited methanogenesis. Radio-isotope studies indicated that the H₂/CO₂ pathway was probably the predominant route for methanogenesis in these sediments through the acetate pathway appeared equally important at the sediment surface. In the absence of sulphate, sulphate reducers probably acted as net hydrogen donors to the methanogens. The process rate was permanently limited by the consistent low temperature (annual range 1–3°C). Rates increased with increasing temperature over the range 4–32°C, but no evidence was found to suggest cold sensitivity or psychrophily. The optimum temperature for methanogenesis was in excess of 30°C, temperatures never experienced at Signy Island. Rates of methanogenesis during the study period (Dec–Mar) ranged from 0.29 to 0.45 mg of carbon m^-2 and on an annual basis methanogenesis was calculated equivalent to 13% of the organic carbon deposition rate.     

Benthic moss pillars in Antarctic lakes

Unique pillar-like colonies of aquatic mosses, rising from cyanobacterial and algal mats, have been discovered in some freshwater lakes in the vicinity of Syowa Station (69°00′S, 39°35′E), continental Antarctica. These moss pillars are about 40 cm in diameter and up to 60 cm high and occur at the lake bottoms mainly between 3 and 5 m depth. The primary component is a species of Leptobryum, a genus unknown in the continental Antarctic terrestrial bryoflora and as an aquatic genus elsewhere in the world. Bryum pseudotriquetrum is often an associated species. In longitudinal section the pillars reveal several whitish layers formed by mineral sediment and dead cyanobacteria. It is speculated that the biomass of aquatic mosses at the bottom of many Antarctic lakes is considerably greater than that previously estimated. Accepted: 11 April 1999     

Protozoan growth rates on secondary-metabolite-producing Pseudomonas spp. correlate with high-level protozoan taxonomy

Different features can protect bacteria against protozoan grazing, for example large size, rapid movement, and production of secondary metabolites. Most papers dealing with these matters focus on bacteria. Here, we describe protozoan features that affect their ability to grow on secondary-metabolite-producing bacteria, and examine whether different bacterial secondary metabolites affect protozoa similarly. We investigated the growth of nine different soil protozoa on six different Pseudomonas strains, including the four secondary-metabolite-producing Pseudomonas fluorescens DR54 and CHA0, Pseudomonas chlororaphis MA342 and Pseudomonas sp. DSS73, as well as the two nonproducers P. fluorescens DSM50090(T) and P. chlororaphis ATCC43928. Secondary metabolite producers affected protozoan growth differently. In particular, bacteria with extracellular secondary metabolites seemed more inhibiting than bacteria with membrane-bound metabolites. Interestingly, protozoan response seemed to correlate with high-level protozoan taxonomy, and amoeboid taxa tolerated a broader range of Pseudomonas strains than did the non-amoeboid taxa. This stresses the importance of studying both protozoan and bacterial characteristics in order to understand bacterial defence mechanisms and potentially improve survival of bacteria introduced into the environment, for example for biocontrol purposes.     

Low temperature constrains growth rates but not short-term ingestion rates of Antarctic ciliates

Low environmental temperature is a major factor affecting the feeding activities, growth rates, and growth efficiencies of metazooplankton, but these features are poorly characterized for most protistan species. Laboratory experiments were conducted to examine the growth and ingestion rates of cultured herbivorous Antarctic ciliates. Three ciliates fed several algal species individually at 0 °C exhibited uniformly low growth rates (<0.26 day^?1), but the algae varied substantially in their ability to support ciliate growth. Specific ingestion rate (prey biomass consumed per unit ciliate biomass per unit time) was strongly affected by ciliate physiological state (starved vs. actively growing). Starved cells ingested many more prey than cells in balanced growth during short-term (minutes-to-hours) experiment but did not grow faster, indicating temperature compensation of ingestion rate but not growth rate. Field experiments were also conducted in the Ross Sea, Antarctica, to characterize the feeding rates of ciliates in natural plankton assemblages. Specific ingestion rates of two dominant ciliates were an order of magnitude lower than rates reported for temperate ciliates, but estimated rates were strongly affected by prey abundance. Our data indicate that short-term ingestion rates of Antarctic ciliates were not constrained by low environmental temperature although overall growth rates were, indicating the need for caution when designing experiments to measure the ingestion rates of these species at low environmental temperature. We present evidence that artifacts arising from estimating ingestion in short-term experiments may lead to errors in estimating feeding impact and growth efficiencies that are particularly large for polar protists.     

Biogeochemical study of organic substances in Antarctic lakes

The features of organic constituents in Antarctic lakes and ponds of the McMurdo, Syowa and Vestfold oases are summarised from a biogeochemical viewpoint. Total organic carbon or dissolved organic carbon contents in saline lakewaters are generally extremely high and much higher than those in freshwater lakes. The concentrations and/or compositions of hydrocarbons, fatty acids, sterols, phenolic acids and hydroxy acids in lake and pond waters and sediments vary markedly, probably reflecting differences in biological activity and source organisms. Long-chain alkenes, such as n-C_29:2 (carbon chain length: numbers of unsaturated bonds) are found as the major hydrocarbons in some anoxic lake sediments. Unusually, long-chain n-alkanoic acids are abundant in some Antarctic lake sediments and 24-ethylcholest-5-en-3-ol is the most prominent sterol in most of the lakes studied. It is suggested that some bacteria, and cyanobacteria and algae are important sources of long-chain n-alkanoic acids and 24-ethylcholest-5-en-3-ol, respectively, as previously reported from environments of the mid and lower latitudes. The dominance of p-hydroxybenzoic acid among the phenolic acids found together with the absence of syringic, p-coumaric and ferulic acids in the Antarctic lakes reflects the absence of vascular plants in the areas studied.In three Antarctic saline lakes (Vanda, Fryxell and Ace) the kinds and amounts of organic constituents differ with depth due to the zonation of microorganisms. The maximum fatty acid contents are found at depths just above the anoxic layer, corresponding to the photosynthetic maxima in the lakes, and the depths of maximum phytoplankton populations. In the bottom sediments of the lakes, the composition of organic substances is significantly different from that in the water columns, indicating that the sinking organic substances are degraded rapidly by microorganisms on the lake bottom.     

Epiphytic diatoms in two freshwater maritime Antarctic lakes

SUMMARY.

• 1 An ecological study of two small maritime Antarctic lakes on Signy Island, South Orkney Islands, was undertaken from January 1986 to March 1987. Analysis of diatom counts from the lakes provided examples of oligotrophic and mesotrophic ecosystems.
• 2 A diverse community of 104 epiphytic taxa was identified. Twenty-eight taxa had a percentage abundance greater than 1% in both lakes. Distinctive dominant taxa were identified from each lake.
• 3 A variety of ordination techniques was performed on the abundance data and a principal components analysis demonstrated differences in the diatom assemblages between the two lakes. Clear separations of sites and species were evident between the lakes, and accounted for the greatest percentage variance.
• 4 Species composition varied with depth within each lake and was also important in influencing changes in assemblage composition between sites.
• 5 A redundancy analysis indicated that species composition was correlated to concentrations of nitrogen and phosphorus but the total variance accounted for by the four physical and chemical factors measured was low (24%).

     

Temperature effects on summer growth rates in the Antarctic scallop, Adamussium colbecki

Annual growth rates of Antarctic marine organisms are low compared to their relatives from warmer waters. Previous studies hypothesise that high food availability during austral spring–summer may enable Antarctic invertebrates to attain comparatively high short-term growth rates despite the low temperature. Neither a temperature-growth experiment with juvenile Adamussium colbecki (Smith 1902) nor the comparison of A. colbecki summer growth rates with an empirical scallop specific growth-to-temperature relationship could confirm this hypothesis. Hence, summer growth rates of young, immature A. colbecki are strongly affected by temperature, i.e. no uncoupling from temperature.     

Light climate and phytoplankton photosynthesis in maritime Antarctic lakes

The responses of phytoplankton populations to seasonal changes in radiation flux in two Antarctic lakes with extensive winter ice-cover are described. A phytoplankton capable of photosynthesis was found throughout the year in both systems. During winter, low incident radiation combined with thick layers of snow and ice prevented in situ photosynthesis becoming detectable. The beginning of spring was marked by a reduction in snow cover which resulted in a considerable increase in surface penetrating radiation. Planktonic algae rapidly adapted to utilise these increased levels efficiently, though they still showed characteristics of strong shade adaptation.Loss of ice cover at the start of the short open water period further increased the radiation levels and a summer population developed which was much less shade adapted. Saturation and photoinhibition effects were widespread during this period as the algae proved unable to utilise high radiation levels efficiently. They were however effective at the radiation fluxes prevalent in the lower part of the rapidly circulating water columns.     

Modelling phytoplankton dynamics in lakes and reservoirs: the problem of in-situ growth rates

During the Surface Water Acidification Programme, ahydrochemical plot study was carried out at thepristine Høylandet study site during 1986–89. Theplot soils were acidic iron podzols (sensuKubiena), with a significant content of secondaryaluminium (Al), forming a potential major source oftoxic Al in streams and lakes. Rain and mist inputscontain small amounts of anthropogenic sulphate, withammonium inputs being enhanced during the summermonths. Vegetation canopy interactions, includingsorption and leaching, change input water chemistrybefore it reaches the soil, in which organicinteractions increase, especially during the summer.Amphibole in the soil parent material is probablyresponsible for the large mineral weathering ratedetermined and this source of base cations, alliedwith the small anthropogenic inputs, results in Alconcentrations in the streamwater being small incomparison with impacted sites.     

Protozoan feeding and bacterial wall growth.

Monod's model is often assumed to describe the kinetics of feeding of a protozoan population on a bacterial population in a chemostat. An earlier study (J. L. Jost et al., J. Bacteriol., 113, 84 (1973)) of the feeding of Tetrahymena pyriformis on either Escherichia coli or Azotobacter vinelandii found that this model correctly predicted the occurrence of sustained oscillations of population densities but made predictions of minimum bacterial population densities that were much smaller than those observed. The earlier study removed the discrepancy between the model and data by replacing Monod's model with a different model. It is shown in the present study that the discrepancy can be explained equally as well if Monod's model for the feed relation is retained and if, in addition, growth of bacteria on the chemostat walls is allowed for in the model equations.     

A method to study bacterioplankton community structure in Antarctic lakes

A method to study bacterioplankton community structure in Antarctic freshwater lake samples is described. Small samples (between 300 and 1000 ml) taken in remote field locations were used for crude DNA extraction, followed by PCR amplification of 16S rRNA gene fragments using group-specific primers. The amplification products of the PCR reaction were then separated using denaturing gradient gel electrophoresis to produce a profile of the bacterioplankton community. Whilst the technique is only semi-quantitative, it readily differentiated communities from lakes of different trophic status and from vertical profiles within different lake types. The method offers a sensitive tool for screening and monitoring Antarctic freshwater environments as a precursor and adjunct to more detailed studies. Accepted: 14 November 1999     

Comparative ecology of plankton communities in seven Antarctic oasis lakes

Similarities and differences in the biological limnology ofseveral perennially ice-covered, amictic lakes within a 100x 100 km grid of an Antarctic desert oasis have been identified.Most of the lakes possessed the cryptophyte Chroomonas lacustrisas the dominant phytoplankter which was accompanied by otheralgae, bacteria, yeasts, and ciliates. Maximum phytoplanktondensities and extractable particulate chlorophyll a usuallyoccurred well below the poorly transparent ice covers. The sevenlakes varied among themselves but all displayed more oligotrophicthan eutrophic values for five trophic state indicators. Thehigh dissolved O₂/CO₂ ratio in these lakes caused by supersaturatedoxygen and the previously reported high proportion of extracellularphotosynthate production by the phytoplankton raise the possibilityof a significant amount of photorespiration compared to inorganiccarbon incorporation for growth. In addition to the supersaturatedoxygen, the plankton communities could be limited by low lightintensities, hypersalinity (in some lakes), available nutrients,and grazing by protozooplankton.     

Viruses in the plankton of freshwater and saline Antarctic lakes

1. Virus‐like particle (VLP) abundances in nine freshwater to saline lakes in the Vestfold Hills, Eastern Antarctica (68° S) were determined in December 1999. In the ultra‐oligotrophic to oligotrophic freshwater lakes, VLP abundances ranged from 1.01 to 3.28 × 10⁶ mL^–1 in the top 6 m of the water column. In the saline lakes the range was between 6.76 and 36.5 × 10⁶ mL^–1. The lowest value was found in meromictic Ace Lake and the highest value in hypersaline Lake Williams. Virus to bacteria ratios (VBR) were lowest in the freshwater lakes and highest in the saline lakes, with a maximum of 23.4 in the former and 50.3 in the latter. 2. A range of morphologies among VLP was observed, including phages with short (Podoviridae) and long tails, icosahedric viruses of up to 300 nm and star‐like particles of about 80 nm diameter. 3. In these microbially dominated ecosystems there was no correlation between VLP and either bacterial numbers or chlorophyll a. There was a significant correlation between VLP abundances and dissolved organic carbon concentration (r=0.845, P < 0.01). 4. The data suggested that viruses probably attack a spectrum of bacteria and protozoan species. Virus‐like particle numbers in the freshwater lakes were lower than values reported for lower latitude systems. Those in the saline lakes were comparable with abundances reported from other Antarctic lakes, and were higher than most values published for lower latitude lakes and many marine systems. Across the salinity spectrum from freshwater through brackish to hypersaline, VLP concentrations increased roughly in relation to increasing trophy. 5. Given that Antarctic lakes have a plankton almost entirely made up of bacteria and protists, and that VLP abundances are high, it is likely that viruses play a pivotal role in carbon cycling in these extreme ecosystems.     

Viral dynamics and patterns of lysogeny in saline Antarctic lakes

Antarctic lakes are extreme ecosystems with microbially dominated food webs, in which viruses may be important in controlling community dynamics. A year long investigation of two Antarctic saline lakes (Ace and Pendant Lakes) revealed high concentrations of virus like particles (VLP) (0.20–1.26 × 10⁸ ml⁻¹), high VLP: bacteria ratios (maximum 70.6) and a seasonal pattern of lysogeny differing from that seen at lower latitudes. Highest rates of lysogeny (up to 32% in Pendant Lake and 71% in Ace Lake) occurred in winter and spring, with low or no lysogeny in summer. Rates of virus production (range 0.176–0.823 × 10⁶ viruses ml⁻¹ h⁻¹) were comparable to lower latitude freshwater lakes. In Ace Lake VLP did not correlate with bacterial cell concentration or bacterial production but correlated positively with primary production, while in Pendant Lake VLP abundance correlated positively with both bacterial cell numbers and bacterial production but not with primary production. In terms of virus and bacterial dynamics the two saline Antarctic lakes studied appear distinct from other aquatic ecosystems investigated so far, in having very high viral to bacterial ratios (VBR) and a very high occurrence of lysogeny in winter.     

Microbial dynamics during the summer ice-loss phase in maritime Antarctic lakes

The dynamics of bacterioplankton and protozooplankton in twomaritime Antarctic lakes (Heywood Lake and Sombre Lake, SignyIsland, South Orkneys) were studied during the phase of icebreak-out (December and early January 1994/95). The lakes aresuffering animal-induced (fur seal) eutrophication, though HeywoodLake is most severely affected. Both lakes had morphologicallydiverse bacterial communities which increased during the studyperiod, reaching maxima of 80 x 10⁸ l^–1 in Heywood Lakeand 31.8 x 10⁸ l^–1 in Sombre Lake. Heterotrophic nanoflagellates(HNAN) reached a peak in late December with maxima of 40.6 x10⁸ l^–1 in Sombre Lake and 174 x 10⁵ l^–1 in HeywoodLake. Phototrophic nanoflagellates (PNAN) peaked in late Decemberafter ice loss in Heywood Lake (63 x 10⁵ l^–1), which coincidedwith a peak in a bloom of Chroomonas acuta which reached abundancesof 1.0 x 10⁸ l^–1. In Sombre Lake, ice persisted for alonger period and here PNAN reached their highest density atthe end of the study period (around 70.0 x 10⁵ l^–1). Ciliateabundance reached high levels in Heywood Lake (>60001^–1),while in Sombre Lake maximum abundance was 568l^–1. Protozooplanktondiversity was greater in the less-enriched Sombre Lake. Grazingrates of ciliates averaged 70.6 bacteria indiv.^–1 h^–1in Heywood Lake and 119.3 bacteria indiv.^–1 h^–1in Sombre Lake. The difference was a reflection of the differenttaxonomic make-up of the community in the lakes. HNAN grazingrates varied between 0.51 and 0.83 bacteria indiv.^–1 h^–1in Sombre and Heywood Lakes, respectively. Specific growth rates(r) h^–1 in Sombre Lake were 0.028 for ciliates and 0.013for HNAN, and in Heywood Lake 0.010 for ciliates and HNAN 0.012.These growth rates result in doubling times ranging between38 and 69 h for ciliates and around 55 h for HNAN.HNAN grazingon bacteria was curtailed in Heywood Lake in early January asa result of predation by microcrustacean larvae feeding on theplankton. Thus, for a short phase top-down control was apparentin the dynamics of Heywood Lake, a feature uncommon in Antarcticlake ecosystems. The impact of natural eutrophication on thesesystems is discussed in relation to other unaffected Antarcticlakes.