Salt Lake

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Microbes exist within all parts of the globe. Where it was once thought that conditions were too extreme to sustain life, microscopic organisms have been found that call it their home and have adapted to such an extreme that they are incapable of survival anywhere else. Salt lakes like the Great Salt Lake in Utah or the Dead Sea along the border of Jordan and Israel are two of the saltiest bodies of water in all of the Earth. These places often accumulate such a high amount of salt and minerals because water runoff towards the lake carries minerals into the lake and when the water evaporates, the salts are left behind and leave the lake even more saline each time. With salt concentrations as much as ten times that of the ocean, these places still manage to maintain microbial life. The organisms that survive use a wide array of strategies to manage the water’s harsh conditions. In order to adapt to the salty environment, halophiles prevent cellular water loss by increasing the intracellular solute concentration in order to reach equilibrium with the extracellular surroundings by adjusting the intracellular concentrations to primarily use potassium as the main cation and synthesizing glycerol to balance the extracellular salt concentration and maintain their membrane stability.

Description of Niche

The Great Salt Lake

Imagine the sun setting over dark wine colored waters. As day turns to night, you marvel at the stillness of your surroundings. While there seems to be very little life, the Great Salt Lake actually teems with all sorts of organisms above and below its surface. This lake has been nicknamed “America’s Dead Sea,” and while there are some obvious similarities between America’s Dead Sea and the Dead Sea, there are far more differences (1). Upon examining both bodies of salty water with an emphasis on the Great Salt Lake, there is the realization that there is more to these waters than meets the eye.

The Great Salt Lake is the fourth largest terminal lake in the world (2). It is also the second saltiest lake in the world; it lacks an outlet so when water enters the lake and evaporates, the salt is left behind (2, 3). Before the construction of a railroad built in 1959, the salt concentration had been fairly homogeneous (2, 4). Upon completion, this railroad separated the Great Salt Lake into two distinct ecosystems with differing organisms and salinity (5, 6, 4). For example, the number of brine shrimp cysts (eggs) in the south arm has decreased while the number of brine shrimp in the north arm has become somewhat unproductive (7).

The South Arm

The south arm has a pH of 8.2 and has a variable salinity due to the various amounts of freshwater entering it (7, 5). It receives ninety percent of the freshwater entering the Great Salt Lake (8). This is important because it affects the salinity and thereby determines the survivability of a number of species in the south arm (5). Recent studies have found that there has been an overall decrease in salinity and an increase in the variety of organisms (4).

The North Arm

One of the most striking features about the north arm is its reddish hue caused by flourishing halophilic Archaea. For this reason, the north arm has been nicknamed the Red Sea (7). Although they are parts of the same lake, physical properties of the north arm and south arm vary by drastic amounts. The north arm has a pH of 7.7 and has fairly stable salinity because it is saturated with salt (7, 5). The north arm is much saltier than the south arm because only ten percent of all the freshwater that enters the Great Salt Lake flows into the north arm (8, 7). Another reason for such high salinity is that the water in the north arm evaporates faster than it enters (3). Because the south arm flows into the north arm, the number of minerals in the south arm has been reduced while the number of minerals in the north arm has been increased (7). The increased salinity has limited the diversity of microbial life capable of surviving (4).

Effects of Salinity Changes

A clear way to describe the effects on ecology of the lake’s changing salinity would be this: the higher the salinity, the fewer species present (3). With the conditions more extreme, fewer species are suited to succeed and grow. The changes in salt levels affect the organisms that live there in many ways and completely transform the ecosystem. High salinity causes brine shrimp to be smaller, reach maturity more quickly and develop a longer abdomen than brine shrimp in less salty water (9). Adult brine shrimp have a maximum salt tolerance around 30% salinity. Cyst (egg) production has optimal levels at around 14% to17%. Interestingly, cysts have evolved to have the following adaptation to their surroundings: they have a lower density in water of 16% to 28% salinity than those in water of 10% to 14% salinity. Cysts break prematurely below these optimal levels (at low salt concentrations). In such conditions, other organisms enter previously uninhabitable areas and consequently affect the ecosystem (9). One example involves the insect Trichocorixa verticalis entering the Great Salt Lake during periods of low salinity (10). At the same time, the number of brine shrimp decreased and three other kinds of zooplankton invaded the area. With the number of brine shrimp decreased, protozoans flourish to fill their role (10).

Lake Effect

The lake effect or – as some like to call it – the “dreaded lake effect” refers to the capricious weather and climate conditions that are influenced by the Great Salt Lake (11). The strength of the lake effect depends on the following: temperature differences between air and lake, more moisture in the air around the lake than the surrounding environment due to lake evaporation and salt particles in the air due to salt from the lake. The temperature differences between air and water predominantly contribute to the lake effect. Such temperature differences are due to the cooling and warming effect of the lake (11). Since temperature differences between air and water are greatest during the months of September through May as well as the fact that the lake warms quickly and its salinity prevents any freezing, the strongest lake effects occur during this time period (11, 12). In addition to this, twice the amount of fog can occur due to overnight cooling of the lake. Winds are also dependent on temperature differences between the air and lake (11)

Heavy Metal Accumulation

Arsenic, copper, cadmium, gold, lead, magnesium, mercury, molybelenum, selenium, silicon, silver and zinc are some common heavy metals found in the Great Salt Lake (11). Such metals enter the lake via streams, rivers and precipitation. Since the Great Salt Lake is a terminal lake, these heavy metals gradually accumulate. The exact impact that the heavy metals have on the ecosystem is unknown, but recent studies on mercury concentrations show that the brine layer in the lake has methylated the mercury (11, 12). While inorganic mercury is toxic, the methylated mercury is even more toxic to organisms because its lipophilic properties allow it to pass the blood-brain barrier. Such methylation allows microorganisms to absorb the heavy metals. Since these microorganisms are at the bottom of the food chain, the organisms higher upon the food chain are also affected (11). High concentrations of selenium and mercury are found in birds such as the common goldeneye, green winged teal and northern shoveler (13). The finding that there is such a high concentration of mercury in the lake is so alarming that even the mainstream media has taken notice, as evidenced by The New York Times article “Studying Great Salt Lake’s High Mercury Levels.” The article can be found here: <http://www.nytimes.com/2008/08/10/science/earth/10saltlake.html>.

The Dead Sea

The Dead Sea is another body of water with extremely high levels of salinity and is very similar to The Great Salt Lake. These places often accumulate such a high amount of salt and minerals because water runoff towards the lake carries minerals into the lake and when the water evaporates, the salts are left behind and become more concentrated each time. Due to irritation for the nearby countries, however, less fresh water flows into the Dead Sea so water evaporates more quickly than it gets replenished and the famous historical landmark is at risk of drying up (28).

Located between Jordan and Israel, this lake is named for its lack of fish and other forms of macroscopic life. With a salt concentration ten times greater than the ocean, the organisms that live there must use unique adaptive measures to survive. Ones that have survived the intense salt levels include species of archaea, bacteria, fungus, and even algae (29).

Who lives there?

Salt-loving organisms known as halophiles are a major part of the salt lake ecosystem. In order to adapt to the salty environment, halophiles prevent cellular water loss by increasing the intracellular solute concentration in order to reach equilibrium with the extracellular surroundings. Halophiles accumulate amino acids, polyols, glycerol, and even KCl to balance the extracellular salt concentration (16). These highly saline conditions in the Great Salt Lake provide an ideal environment for many living organisms, including haloarchaea, green algae (Dunaliella salina), cyanobacteria (Aphanothece halophytica), brine shrimp, brine flies, Corixids, millions of various species of shorebirds, as well as the following specific species of halobacteria: Micrococcus subflavus, Bacillus mycoides, Achromobacter harteibii, and Bacterioides rigidus, to name a few (17). The organisms inhabiting the Great Salt Lake range from the primary producers or microbes to the consumers. Both the producers and consumers contribute to this hypersaline ecosystem (17).

Producers

The primary producers in the Great Salt Lake include green algae and halophilic archaea. Although the time of year determines which type of eukaryotic halophilic algae is more abundant, primarily Dunaliella viridis is observed in bloom in the lake’s south arm, while Dunaliella salina is most abundant in the lake’s more saline north arm (17). The algae are a substantial food source for the brine shrimp and brine flies that inhabit the lake. Dunaliella utilize polyols, primarily glycerol, in order to balance the intracellular solute concentration and prevent osmotic stress caused by the salty environment (16). Dunaliella salina require saturated salt concentrations (up to 5 M NaCl) in order to grow at a maximum rate. Due to Dunaliella salina’s propensity to synthesize beta-carotene, the northern arm of the lake can appear red at times (17).

Halophilic archaea are commonly found in environments with high salt concentrations, ranging from 3.4 - 5 M, like that of the Great Salt Lake (18). Haloarchaea exist in a variety of shapes, including rod, cocci, disc, triangular, and square (18). Some even appear purple in color due to the presence of bacteriorhodopsin, which functions as a proton pump dependent upon light for proper function. This proton pump aids in the generation of ATP for archaea (19). Some haloarchaea proteins have adapted to the high salinity of the Great Salt Lake by becoming resistant to the salty environment. Other halophilic archaea proteins actually demand high salt concentrations for activation (19). Haloarchaea manage the intense salt concentrations of the lake due to evolutionary features, which include: their ability to ferment many different types of sugars, to grow by utilizing nitrate reduction and denitrification, as well as by using single carbon sources including acetate, glycerol, and other sugars to balance the osmotic strain due to the environment’s salinity (18).

Similar to the halophilic algae of the lake, the archaea also synthesize carotenoids and beta-carotene, which facilitates the repair of UV-damaged thymine dimers. Light-dependent chloride pumps and retinal proteins enable archaea to swim towards green light, but away from harmful UV light. Both aerobic and anaerobic species of haloarchaea exist (18). Aerobic haloarchaea use gas vesicles in order to adapt to their environment, which allow the archaea to float to the water’s surface where oxygen is more abundant. This is necessary for aerobic archaea that require higher concentrations of oxygen for survival (18). Anaerobic haloarchaea can be observed on the lake’s sediment bottom. These anaerobes synthesize acetate from the oxidation of sugars (18).

In order to tolerate the salt concentration in the extracellular environment, archaea use a sodium-potassium pump. The sodium-potassium pump monitors intracellular and extracellular ion concentrations, balancing osmotic pressure by pumping out sodium ions and retaining potassium ions. Glycerol is synthesized or sequestered to maintain this osmotic balance (19).

Among the microbes living in the Great Salt Lake, many fungi and yeasts have also evolved to survive the harsh salt environment, but are primarily aerobes. An example of halophilic yeast is Debaromyces hansenii, as it is able to grow in an aerobic environment with salt concentrations reaching 4.5 M (16). Similar to the haloarchaea, this yeast uses glycerol, as well as arabitol to the maintain osmotic pressure between the inside and outside of the cell. Glycerol is produced at the log growth phase, while arabitol is synthesized during the stationary phase when the growth rate has stabilized (16).

Consumers

Artemia or brine shrimp are an important part of the Great Salt Lake ecosystem. Brine shrimp are small crustaceans measuring nearly 15 mm in length and located in hypersaline environments. Both Artemia fraciscana and Artemia salina reside in the Great Salt Lake (20). Brine shrimp eggs can survive for a long period of time in a dry, cyst state. Because of this feature, brine shrimp eggs are commonly sold commercially as food for fish and other aquarium animals (17). These small crustaceans swim upside down and feed on the green algae in the environment (20). The adult brine shrimp consume phytoplankton in the lake and diatoms (17).

Brine flies, primarily the Ephydra cinerea and Ephydra hians species, greatly contribute to the food chain of the Great Salt Lake. Although their lifespan is only about 3-5 days long, they are an important part of the lake’s ecosystem, as they are the primary food source for the numerous shorebirds the lake attracts (17). The Ephydra cinerea species dominates the northern arm of the lake, while the Ephydra hians thrives in the south arm. Both feast on the algae and bacteria that accumulate on the rocks (17). Brine flies require oxygen in order to survive and obtain sufficient amounts from algal photosynthesis. The brine flies appear on the water’s surface beginning in the pupae phase of development due to air bubbles that enable floatation (17).

A species of insect known as Tricorixia verticalis can also be found in the Great Salt Lake. Tricorixia are water bugs, measuring only 13 mm in length, commonly referred to as “water boatmen” (17). This triangular-headed insect feeds on both brine shrimp and brine fly larvae and resides near the bottom of the lake. When feeding, the water boatmen inject saliva into the algae with their straw-like mouths, which allows for easier digestion (20).

Current Research

Haloarchaea Viruses

Viruses whose effects are exclusive to haloarchaea are known as haloarchaea viruses (sometimes halophages or haloviruses). A large portion of research conducted on halophages to date has been relatively slow in comparison to other bacteriophages. The issue that serves as the largest obstacle in the study of haloarchaea viruses is the ability to grow halobacteria host cells, particularly those that are most dominant in the salt water bodies. To date the most well studied haloarchaea virus is the ΦH strain, being the few haloviruses to have had its genome sequence studied in depth. The study of halophages, though relatively slow, is nonetheless of very high interest especially pertaining to large saline bodies of water like the Dead Sea, where the halovirus count can be as high as 10,000,000/mL.

Genetic Similarities Between Phages

Although their local surroundings are often very different, halophages share many traits with mesophilic bacteriophages. In the case of comparing the well studied lyosogenic ΦH halovirus (which infects Halobacterium salinarum) with P1 bacteriophages, both share traits in morphology, replication, and lysogenic techniques. Although both groups share many functional similarities, strangely enough genome sequencing determined neither group has close genetic ties to each other (21).

On the other hand, when the ΦH halovirus is compared with its close cousin the ΦCh1 halovirus, many functional differences exist between the two. While the ΦH virus inhabits haloarchaea, the ΦCh1 choose its targets to be haloalkaliphiles, thus underscoring the inconsistent relationship between genetic relatedness and functional similarity. Study of the evolution in the viruses goes on to explain the apparent inconsistent relationship between genetic relatedness and functional differences.

Survivability in Salt Deposits

In an attempt to explore the extent of survivability of halobacteria in a salt crystal environment, cultures of haloarchaea were grown and simulations of evaporate formation were conducted. Extractions of the cells were done, yielding different percentages of cell survival, ranging from 0.4% to 16.0% depending on phylotype (24). Cells that were stained prior to being place in the cells indicated a majority of the cells clustered themselves in the fluid inclusions within the salt crystal. (22 & 25)

Researchers at the University of California, Berkeley also conducted Martian-climate simulations on samples of highly halophilic Haloferax volcani, obtained from the San Francisco Bay. Able to withstand up to 30% NaCl, the samples were subjected to a setting 5 torrs of pressure and a local temperature of -27OC. Over the course of eight months the cell density of the samples in Martian-like conditions dropped from 2.2x106 to 4.2x105 Colony Forming Units (CLU) per mL. Much like the study conducted in Austria there was an expected drop of CLU but were able to survive nonetheless, although the simulation temperature of -27OC is far higher than the actual temperature of -70OC on the surface of Mars. (26)

Mars as a habitat

Scientific speculation as to the kind of life that existed on Mars has led to the belief that types of haloarchaea have once and may still exist on the planet. Current whereabouts of haloarchaea on Mars has been speculative but there have been cases of halobacteria being able to survive 300 million years in salt crystals in the Austrian Alps (1), fueling the notion that haloarchaea dating back from Mar’s era of life ~3.5 billion years ago could still be viable and taking refuge in salt crystals (22 & 23).

There have been numerous events that have suggested Mars would provide a suitable habitat for haloarchaea. Samples of meteorites originating from Mars have been shown to contain amounts of halite, sodium chloride in its mineral form. Studies carried out by NASA in the exploration of Mar’s planetary surface suggests that salt water deposits do exist, suggesting in the past that Mars once had a saline environment that could have been suitable for halophiles. (26)

In order to observe the sustainability of the halophiles under present-day Martian conditions, salt deposits implanted with samples of Halococcus dombrowskii and Halobacterium salinarum were placed in Mars-climate simulators. Placement in the simulator over a period of a month resulted in cells sustaining life though there was a decrease in cell count, desiccation occurred, and damage to genetic sequence of cells; the presence of brine substantially retarded the decrease in cell count by as much as a factor of 10 (24). It has been proposed that haloarchaea can survive in Martian conditions while in a dormitory phase, even though sporulation is not a trait that is typically seen in them. Although only observable for some strains, certain haloarchaea have the ability to go into a resting phase whereby a cyst is formed around the cells (22), most likely providing an extra layer of isolation and protection against the environment.

There is skepticism as to whether haloarchaea that existed during the planet’s era of life (nearly four billion years) could have survived till this present day. It has been argued that the much lower temperature existing on the planet would allow for halophiles in salt deposits to be preserved well enough. Sustainability of haloarchaea on Mars would only be pragmatically possible if the halophiles had acquired adaptations to counter low temperatures and were buried low enough underground to be shielded from UV rays that would otherwise damage DNA (22) and quite possibly protein structure.

Closing Thoughts

At first glance, the Great Salt Lake and the Dead Sea do not seem to be particularly interesting. A closer inspection, however, reveals that the lake is rich in biological diversity. While there certainly is a wealth of information about these salt lakes, there is still much to be learned about them. Current and future research will help unfold the lake’s mysteries.

References

1) Arave, L. “Great Salt Lake – a lively recreational jewel.” Deseret News. 1 Aug. 1999. <http://deseretnews.com/misc/gsl/100013637.htm>.

2) Baxter, B., et al. “Microbial Diversity of Great Salt Lake.” Cellular Origin, Life in Extreme Habitats and Astrobiology. 28 Dec. 2005: 9. Adaptation to Life at High Salt Concentrations in Archaea, Bacteria, and Eukarya. Netherlands: Springer Netherlands, 2006.

3) Stephens, D. and Gardner, J. “Great Salt Lake, Utah.” USGS Water-Resources Investigations Report 99-4189. Apr. 2007. <http://pubs.usgs.gov/wri/wri994189/PDF/WRI99-4189.pdf>.

4) Rushforth, S. and Felix, E. “Biotic Adjustments to changing salinities in the Great Salt Lake.” Microbial Ecology 8.2 (1982): 157-161.

5) “Facts - Lake Properties.” Great Salt Lake Ecosystem Program. 2008. <http://wildlife.utah.gov/gsl/facts/properties.php>.

6) Stephens, D. “Changes in lake levels, salinity and the biological community of Great Salt Lake (Utah, USA), 1847-1987.” Hydrobiologia 197.1 (1990):139-146.

7) Post, F. “The microbial ecology of the Great Salt Lake.” Microbial Ecology 3.2 (1977): 143-164.

8) “Brine shrimp – Brine shrimp in the North Arm.” Great Salt Lake Ecosystem Program. 2008. <http://wildlife.utah.gov/gsl/brineshrimp/north_arm.php>.

9) “Brine shrimp – What are the effects of salinity?” Great Salt Lake Ecosystem Program. 2008. <http://wildlife.utah.gov/gsl/brineshrimp/salinity.php>.

10) Wurtsbaugh, W. “Food-web modification by an invertebrate predator in the Great Salt Lake (USA).” Oecologia 89.2 (1992): 168-175.

11) “Facts – Heavy Metals.” Great Salt Lake Ecosystem Program. 2008. <http://wildlife.utah.gov/gsl/facts/heavy_metals.php>.

12) Naftz, D., Waddell, B., Krabbenhoft, D. “Mercury in water and biota from Great Salt Lake, Utah: Reconnaissance-phase results.” USGS. Feb. 2005. Utah Department of Environmental Quality. 2008. <http://www.deq.utah.gov/Issues/GSL_WQSC/docs/related_fact_sheets/ASLO-Hg-poster-JAN05.pdf>.

13) Vest, J. et al. “Trace Element Concentrations in Wintering Waterfowl from the Great Salt Lake, Utah.” Archives of Environmental Contamination and Toxicology (2008).

14) Naftz, D., Waddell, B., Krabbenhoft, D. “Mercury in water and biota from Great Salt Lake, Utah: Reconnaissance-phase results.” USGS. Feb. 2005. Utah Department of Environmental Quality. 2008. <http://www.deq.utah.gov/Issues/GSL_WQSC/docs/related_fact_sheets/ASLO-Hg-poster-JAN05.pdf>.

15) Vest, J. et al. “Trace Element Concentrations in Wintering Waterfowl from the Great Salt Lake, Utah.” Archives of Environmental Contamination and Toxicology (2008).

16) Department of Botany. Life in the Great Salt Lake. Weber State University. <http://facutly.weber.edu/sharley/AIFT/GSL-Life.htm>.

17) Boone, D. and Reysenbach, A. Archaea: Diversity. 2003. Wiley InterScience.

18) Allred, A. and Baxter, B. Microbial Life in Hypersaline Environments. Microbial Life Educational Resources. <http://serc.carleton.edu/microbelife>.

19) Brine shrimp. 2008. Encyclopedia Britannica Online. 21 August 2008 <http://www.search.eb.com/article-9016469>.

20) Corixid. 2008. Encyclopedia Britannica Online. 21 August 2008. < http://www.britannica.com/EBchecked/topic/636982/water-boatman>.

21) Dyall-Smith, M., Tang, S., & Bath, C. (2003). Haloarchaeal viruses: how diverse are they? Research in Microbiology 154, 309–313.

22) Stan-Lotter, H., Radax, C., Legat, A., Pfaffenhuemer, M., Wieland, H., Leuko, S., Weidler, G., Ko, N., & Kargl, G (2003). Astrobiology with haloarchaea from Permo-Triassic rock salt. International Journal of Astrobiology 1 (4), 271–284.

23) Landis, Geoffrey A (2001). Martian Water: Are There Extant Halobacteria on Mars?. Astrobiology 1 (2), 161-164.

24) Radax, C., Wieland, H., Pfaffenhuemer, M., Leuko, S., Rittmann, S., Weidler, G., Gruber, C., Stan-Lotter, H. (2003). Microbial Biodiversity in Alpine Permo-Triassic Rock Salt. Geophysical Research Abstracts 5, 09354.

25) Leuko, S., Legat, A., Fendrihan, S., Wieland, H., Radax, C., Gruber, C., Pfaffenhuemer, M., Weidler, G., Stan-Lotter, H. (2005). Isolation of Viable Haloarchaea from Ancient Salt Deposits and Application of Fluorescent Stains for in situ Detection of halophiles in Hypersaline Environmental Samples and Model Fluid Inclusions. Adaptation to Life at High Salt Concentrations in Archaea, Bacteria, and Eukarya, 91-104.

26) Chu, H., & Sheng, W. (2002). Exobiology: The Survival Ability of Halophiles under Martian Conditions. University of California at Berkeley, Earth and Planetary Science Dept.

27) H. Stan-Lotter, H., S. Fendrihan, S., Leuko, S., Legat, A., Gruber, C., Pfaffenhuemer, M., Weidler, G., Busse, H.-J (2005). Survival of halobacteria (haloarchaea) in fluid inclusions as a model of biotic survival in subterranean and extraterrestrial halite. Geophysical Research Abstracts 7, 09129.

28) Jordan Tourism Board. "Eco and Nature". Visit Jordan. 29 August 2008.Jordan Tourism Board. 29 August 2008 <http://www.visitjordan.com/visitjordan_cms/MajorAttractions/TheDeadSea/EcoNature/tabid/141/Default.aspx>

29) Oren, Aharon. "Microbiology and Biogeochemistry of Hypersaline Environments". CRC Press 1998

Edited by Alan Wong, Gary Porter, Kate Graham, Nicolle Ma, students of Rachel Larsen