Literature Review

The purpose of this paper is to explore current literature on the cyanobacteria genus Euhalothece, and to describe the genetic adaptations that enable it to survive in hypersaline lacustrine environments. Additionally, the importance of Euhalothece as a primary producer in these ecosystems, specifically in the benthic zone in the south arm of Great Salt Lake, Utah, is emphasized. Euhalothece is the dominant contributor to the formation of microbialites, organo-sedimentary structures consisting of microbial mat communities that provide food and habitat for the lake’s primary consumers. The decline of Great Salt Lake resulting from many factors, including the ongoing megadrought affecting the Western United States, anthropogenic climate change, and diversion of freshwater inflow for agricultural use, threatens Euhalothece and subsequently the entire benthic food chain. The restoration of lake levels and recovery of microbialites are necessary to prevent the collapse of the ecosystem.

Introduction to Cyanobacteria

Cyanobacteria are a large phylum of genetically diverse phototrophic prokaryotes. Their name comes from the Greek word for blue, kuanós, in reference to the pigments they use to capture energy from light during photosynthesis. This occurs within the thylakoid, an internal membrane lacking in heterotrophic prokaryotes (Liberton et al., 2013). Phototrophic eukaryotes have thylakoid membranes within organelles called plastids, such as chloroplasts in green plant cells. These organelles likely arose as a product of endosymbiosis between early cyanobacteria and prokaryotic cells (reviewed in McFadden, 2001). 

  Cyanobacteria are widespread in almost all terrestrial and aquatic environments, including soils, rocks, lichens, lakes, and oceans, as well as in extreme environments such as geothermal hot springs, hypersaline lakes, and Antarctica (De Los Ríos et al., 2007). Due to their abundance, cyanobacteria play a major role in the primary production of biomass and global oxygen. They are the oldest known oxygen producers and are thought to have caused the Great Oxidation Event—the conversion of the early reducing atmosphere to an oxidizing one—about 2.4-2.1 billion years ago (Gumsley et al., 2017). Indeed, the oldest fossils identified are of microbial mat structures called microbialites that have been dated about 3.7 billion years old.

Modern microbialites exist today in extreme environments such as the hypersaline waters of Shark Bay, Western Australia, and Great Salt Lake, Utah. The study of these structures in hypersaline environments that has led to the discovery of the novel cyanobacteria genus, Euhalothece.

1. Hypersaline Cyanobacteria
2. Morphology

Euhalothece is a genus of unicellular halophilic bacteria of the order Chroococcales. Cell size and shapes are dependent on environmental conditions (Bhatt et al., 2016) and they vary between oval and rod shapes, typically measuring between 2.0 to 6.0 μm in width but can reach up to 18 μm long and 14 μm wide under nutrient-rich conditions (Mogany et al., 2018). They store photosynthetic pigments chlorophyll a and b and C-phycocyanin (C-PC) between numerous irregular thylakoids, resulting in the characteristic dark blue-green coloration.

Individual cells can adjust their buoyancy, sinking to access nutrients and floating to access sunlight; this ability lessens with age and older cells remain close to the surface. They produce a thin exopolysaccharide (EPS) slime layer that adheres to the cell wall. This allows them to form biofilms and protects against environmental stresses such as desiccation, UV radiation, osmotic shock, and pH shifts (Fleming, 1993), as well as high salinity. (Yang et al, 2020). The rate of EPS production increases in response to rising salinities (Ozturk and Aslim, 2010). 

Fig 1. Euhalothece micrographs. (A) Light microscopy of cells undergoing binary fission, (E) SEM showing EPS between cells (adapted from Mogany et al, 2018)

1. Molecular Biology

In addition to producing EPS, Euhalothece has several other genetic adaptations for thriving in hypersaline environments, including genes that code for the synthesis of carotenoid-binding proteins EuOCP and EuHCP (Yang et al., 2020). As the name suggests, these proteins bind carotenoids: powerful antioxidants that scavenge reactive oxygen species to prevent salt stress-induced oxidative damage. In addition, multiple genes code for the production and accumulation of compatible solutes that act as osmoprotectants such as glycine betaine, sucrose, trehalose, and proline (Klähn et al., 2010; Pade and Hagemann, 2015). Osmoprotectants allow the cells to regulate the osmotic pressure of their hypersaline environment. Additional adaptations include resistance to heavy metals such as cadmium, mercury, and arsenic, as well as carbon, phosphorus, and nitrogen fixation (Mogany et al., 2018).

2. Ecology

Euhalothece can be found widespread in hypersaline lacustrine and marine environments (Oren, 2015; Mogany et al. 2018). An environment is considered hypersaline when salinity is above that of seawater, which averages 35 g/L or 3.5%, up to and including salt saturation. Euhalothece is an obligate moderate halophile, tolerating salinities between 6-15% with optimal growth occurring at 12%. Ideal conditions also include pH 8.5 and temperatures between 30-40°C. Along with other cyanobacteria, they are the primary producers in these habitats. One such place Euhalothece dominates biomass production is Great Salt Lake (GSL), Utah.

GSL is a large terminal lake located in the northern part of Utah, USA. It’s the largest lake in the western United States as well as the fourth largest meromictic lake and eighth largest endorheic lake in the world (Keck and Hassibe, 1978; Shroder et al., 2016; reviewed in Lindsay et al., 2020). It’s a remnant of Lake Bonneville, a Pleistocene freshwater lake that rapidly drained approximately 14,500 years ago in a catastrophic flooding event (Malde, 1968). Subsequent evaporation of water that remained concentrated relict minerals, forming the modern hypersaline GSL. It is the world’s second saltiest lake after the Dead Sea (Shroder et al., 2016). In 1959, a railroad causeway was constructed to replace the wooden trestle previously in use to allow the Central Pacific Railroad to cross (Cannon and Cannon, 2002). This effectively divided the lake, reducing water exchange among the two halves and creating an artificial salinity gradient between the north arm (NA) and south arm (SA). The SA receives 95% of freshwater inflow to the lake from the Bear, Jordan, and Weber rivers (reviewed in Lindsay et al. 2020). The resulting salinity averages 11-14%, considerably less than the NA at 24-31%. This range is optimal for Euhalothece, which dominates the lake’s primary production in both the pelagic and benthic zones, the latter of which is heavily comprised of microbialites (Lindsay et al, 2017), which cover more than 20% of the SA’s littoral zone, approximately 260 km² (Wurtsbaugh et al., 2011).

Microbialites are organo-sedimentary structures formed through the mediation of benthic microbial communities (Wurtsbaugh et al., 2011), primarily photosynthetic cyanobacteria and diatoms. When carbon dioxide (CO₂) is dissolved in water, it forms carbonic acid (H₂CO₃), lowering the surrounding pH. This in turn dissolves minerals in the water column, such as calcium carbonate (CaCO₃). H₂CO₃ is consumed during photosynthesis which increases pH and promotes the precipitation of CaCO₃, which contributes to microbialite structure in two forms: oolitic sand—layers of CaCO₃ built up around mineral or brine shrimp fecal pellet cores (Gwynn, 1996;)—and aragonite grains (Lindsay et al., 2017; Dunham et al., 2020). These are trapped in EPS secreted by Euhalothece and other species of cyanobacteria. Over time, the structure is accreted into a characteristic dome, with many domes coming together to form substantial complexes often compared to coral reefs (Riding, 2000; Lindsay et al., 2017). Much of the microbial community is situated on the surface of the dome in a thick biofilm, of which Euhalothece comprises 12% and is the dominant primary producer.

Fig 3. Microbial mats (photo Credit: B. Baxter)

Primary production in GSL supports two primary consumers: brine shrimp (Artemia franciscana) and brine flies (Ephydra spp.). A. franciscana primarily feeds on planktonic algae and cyanobacteria (Belovsky et al., 2011) while Ephydra larvae graze on microbialites in the benthic zone (Collins, 1980), which also provide a surface for anchoring their pupae during metamorphosis (Wurtsbaugh et al., 2009). These two macroinvertebrate species in turn support many secondary and tertiary consumers, including many of the 10 million birds that visit GSL annually for nesting and refueling (Sorensen et al., 2020). The linear nature of this food chain suggests a strong dependency on the primary producers, the loss of which would result in a collapse of the entire ecosystem (Lindsay et al., 2019).

Fig 4. (left) benthic food chain; (right) pelagic food chain (used with permission from Great Salt Lake Institute at Westminster College and Genetics Science Learning Center at the University of Utah )

GSL is in rapid decline largely due to the current diversion of freshwater inflow to the lake for human consumptive use, primarily agriculture (Null and Wurtsbaugh, 2020). This has resulted in a loss of 48% of lake volume and 50% of surface area (Lindsay et al., 2019). Furthermore, natural evaporation cycles have been compounded by the decades-long megadrought affecting the Southwestern United States, exacerbated by anthropogenic climate change (Williams et al., 2022). The receding lake level has resulted in the mass exposure of 40% of SA microbialites, which bleach as the microbial mats desiccate (Frantz et al., unpublished data). Endolithic communities persist for some time and can recover the microbialite upon rehydration, but if the microbialite has been exposed for long enough the endolith will die, resulting in a collapse of the dome and destruction of the microbialite. Additionally, the loss of lake water leads to a rise in salinity; the SA approached 20% in 2022 (USGS, 2023) Primary production in the lake drops as salinity rises, with primary producers, including Euhalothece, dying off between 15-20% (Lindsay et al., 2019). Salt stress also affects the invertebrates and brine fly habitat is lost as the microbialites are beached and dried (Abbot et al., 2023). These factors will result in a substantial loss of A. franciscana and Ephydra and the collapse of the ecosystem. 

Fig 5. Bleached microbialite dome (photo Credit: B. Baxter)

3. Conclusion

As an obligate halophile, Euhalothece possesses several adaptations that allow it to thrive under conditions of desiccation and salt and stress, including EPS production and the accumulation of osmoprotectants (Klähn et al., 2010; Pade and Hagemann, 2015; Mogany et al., 2018). It plays a significant part in primary production within hypersaline lacustrine environments, including the SA of GSL where it serves as the foundation for the benthic food chain as part of microbialite communities (Lindsay et al., 2017). Ephydra larvae use microbialites as both a food source and point of attachment for their pupae. As an extreme environment, GSL has a limited number of primary producers to support its ecosystem. While Euhalothece can tolerate salinities up to 15% (Mogany et al., 2018), the SA approached 20% in 2022 (USGS 2023) as a result of the ongoing loss of lake volume. The prolongation of high salinity, along with mass microbialite exposure, will devastate the ecosystem unless lake levels can be restored and the microbial mats recovered.

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Caitlin Christensen graduated from Westminster College in 2023 with a BS in Biology. She is interested in microbiology and all things relating to Great Salt Lake.