A Contaminating Diversification: Discovering New Algal Toxins in Our Oceans and its Negative Implications

By Casey Dresbach, SRC intern

Coastal waters are one of the world’s greatest assets, yet they are being hit with pollution from all directions (U.S. Commission on Ocean Policy, 2004). As we move further into the Anthropocene, water conditions worldwide are continuing to degrade. The U.S. Environmental Protection Agency’s (EPA’s) 2002 National Water Quality Inventory found that just over half of the estuarine areas assessed were polluted to the extent that their use was compromised (U.S. Commission on Ocean Policy, 2004). Urban wastewater treatment plants, storm runoff, agricultural runoff, and animal feeding operations, are just some of the many sources in which our waters are faced with anthropogenic pollutants (See Figure 1). Eutrophication is the process by which water bodies are made more eutrophic through an increase in their nutrient supply (Smith, Tilman, & Nekola, 1999). Not only does this process cause damage on an ecological level, but it can have implications on economic impacts as well (U.S. Commission on Ocean Policy, 2004). Some of which include beach closures and severe increases in health care costs. It is the leading pollution problem that both humans and animals are facing.

Toxin Microcystin in the blue-green algae in Discovery Bay, California. Human exposure to such toxin may include dizziness, rashes, fever and vomiting.) (McClurg/KQED, 2016).

In a recent study, the San Francisco Bay (SFB) was analyzed on behalf of its responsibility for Harmful Algal Blooms (HABs) in its eutrophic estuary (Peacock, Gibble, Senn, Cloern, & Kudela, 2018). As mentioned earlier, eutrophication as a result of human induced nutrient inputs from growing urban lifestyles are increasing the frequencies of HABs. This study looked into the presence of four harmful algal toxins present in SFB’s specifically within the marine mussel, Mytilus californianus. The toxins found came from both marine and freshwater sources, an alarming discovery. “The bay is acting as a big mixing bowl where toxins from both fresh and marine water are found together,” said senior author Raphael Kudela, the Lynn Professor of Ocean Health at UC Santa Cruz. “A big concern is that we don’t know what happens if someone is exposed to multiple toxins at the same time.” (Peacock, Gibble, Senn, Cloern, & Kudela, 2018).

The four toxins found were Domoic acid, Saxitoxins, Dinophysis, and Microcystin. Domoic acid is a neurotoxin that causes amnesic shellfish poisoning in humans and is produced by marine diatoms. Saxitoxins are paralytic and primarily found in shellfish. Dinophysis are also shellfish toxins that cause severe diarrhetic poisoning. Microcystins are produced by freshwater cyanobacteria and can cause liver damage in both humans and animals. (Peacock, M. B., Gibble, C. M., Senn, D. B., Cloern, J. E., Kudela, R. M., 2018). The study was also conducted during a severe drought in California, which could have brought some of these marine toxins further into the bay due to less freshwater river flow.

NASA uses airborne remote imaging spectrometer to create maps of San Francisco Bay showing water clarity (turbidity), dissolved carbon, and Chlorophyll-a. as indicators of water quality). (NASA/Jet Propulsion Laboratory, 2016).

The presence of the toxins indicated that both the mussels and humans who consume them are exposed to poisoning at both sub-lethal and acute levels. The findings showed that 99% of the mussels collected from SFB were contaminated with one of the listed toxins and 37% had all four. Although alarming, the results served as a progressive measure towards changes and monitoring programs within several federal agencies (Peacock, Gibble, Senn, Cloern, & Kudela, 2018). The other important variable, the drought environment in which this study was conducted, is also important to consider. NASA recently published a study on behalf of their monitoring of SFB’s quality of freshwater (NASA/Jet Propulsion Laboratory, 2016). They demonstrated how an airborne environmental monitoring instrument could be useful in helping monitor not only estuarine waters native to California, but coastal waters worldwide (See Figure 2).

When studies such as these are published, it is dire for the public to grasp the central purpose of such examinations especially in the cases of eutrophication, which affect both humans and animals worldwide. Unfortunately, harmful algal blooms are assuming a more normative nature and its long-term implications absorbed by both humans and animals are not entirely understood. More research needs to be done in this sector specifically, especially when dealing with lethal and sub-lethal levels of toxins within our communities worldwide. The findings also suggest the need to better monitor both marine and freshwaters, similar to what NASA did with their study in the estuary of SFB (NASA/Jet Propulsion Laboratory, 2016).

Overall, deeper analyses should be performed in collaborative measures to incorporate a sense of inclusivity from both the public and scientific sector. Published science is readily available, however it is the proper dissemination of knowledge to human populations outside of the scientific community that is lacking. Without a fertile middle ground to interpret the specificity of what is going on in a world threatened by pollution, policy work, legal intervention, and preventative measures will be challenging to attain. Reducing water pollution will alleviate a series of pressures on both an ecological and economic scale. Cleaner coastal waters and healthy habitats for aquatic life should continue to be the primary concern for policy makers in modern marine affairs.

Works Cited

McClurg/KQED, L. (2016, August 29). Poisonous Algae Blooms Threaten People, Ecosystems Across U.S.

NASA/Jet Propulsion Laboratory . (2016, February 29). NASA demonstrates airborne water quality sensor.

Peacock, M. B., Gibble, C. M., Senn, D. B., Cloern, J. E., & Kudela, R. M. (2018). Blurred lines: Multiple freshwater and marine algal toxins at the land-sea interface of San Francisco Bay, California. Harmful Algae , 73, 138-147.

Smith, V. H., Tilman, G. D., & Nekola, J. C. (1999, March 22). Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environmental Pollution.

U.S. Commission on Ocean Policy. (2004). An Ocean Blueprint for the 21st Century Chapter 14: Addressing Coastal Water Pollution. Washington: University Press of the Pacific.

Bioactive Compounds Derived from Marine Algal Species


By Kyra Hartog, RJD Intern

1. Introduction

Marine algal species produce a variety of compounds that are ultimately beneficial to human health. These compounds are often produced as secondary metabolites [1], meaning they are not essential to the algal species’ survival but benefit the organism in some way. These compounds include, but are not limited to, polyunsaturated fatty acids and carotenoids, as well as compounds with antibiotic and antifungal activity. Those compounds with antibiotic and antifungal activity are being investigated for use as components in anti-fouling paints for maritime industries around the world [1]. Polyunsaturated fatty acids are being studied in relation to their benefits to human health including their potential anticancer activity [2] and their potential for treatment of the symptoms of cystic fibrosis [3]. Carotenoids also have great potential for benefits to human health including treatment of degenerative diseases like macular degeneration and the development of cataracts [4, 5]. Both polyunsaturated fatty acids and carotenoids can be found in algal species, which may provide a less expensive, more efficient mode of production for these compounds [6, 7]. Various algal species are also being studied as bases for biofuels that are more sustainable than current terrestrial options including oil palms, corn, and sugar cane [8].

Though marine products appear to have limited historical use as herbal remedies and medicinal products, a few instances have been reported in the case of marine algal species. Algal metabolites have been studied and developed further as technology to extract and bioassay these metabolites has developed. Marine algae are defined as eukaryotic macroalgae and microalgae for the purpose of this review. Prokaryotic “blue-green algae” (Cyanobacteria) are beyond the scope of this review.

2. Historical use of algae as herbal remedies and supplements

Of the many plant-based herbal remedies used throughout history, only a few have been derived from algal species. Inuit tribes in Nunavut, Canada used parts of a brown algae Laminaria solidungula as a general health supplement [9]. Members of the Rhodophyta division, Chondrus crispus and Mastocarpus stellatus, were used in Irish folk medicine as part of a beverage popular for treating colds, sore throats, and chest infections, including Tuberculosis [10]. They were also boiled in milk or water as remedies for burns and kidney issues [10]. Juice from another red algae, Porphyra umbilicalis, was used as a cancer remedy, particularly breast cancer. It was also used in the Aran Islands as a remedy for indigestion in people and constipation relief in cows [10].

3. Polyunsaturated Fatty Acids (PUFAs)

One typically thinks of marine polyunsaturated fatty acids (ω-3 and ω-6) as coming from oily fish like salmon and anchovies. Marine microalgae also represent a great source of these long chain PUFAs including docosahexaenoic acid (DHA) and eicosapentanoic acid (EPA) which play several important roles in the human body. DHA has been linked to brain development support in infants and may offer other protective functions to the brain later in life [11]. EPA gives rise to anti-inflammatory eicosanoids, which play crucial roles in the immune system, cardiovascular function, and cell communication in general [12].

3.1. PUFAs and Cancer

Marine derived PUFAs have three potential avenues for use in relation to cancer treatment: as an adjuvant for chemotherapy treatment, as compounds with direct anti-cancer effects, or as supplements to ameliorate the secondary effects of radiation and chemotherapy treatments [2]. The direct anti-cancer effects are specifically against tumors through inhibition of angiogenesis and metastasis [13]. These PUFAs were originally thought to have anti-cancer activity due to the low incidences of cancer reported in areas like Japan and the Mediterranean, where n-3 and n-6 levels are high in the diet [14]. The anti-inflammatory nature of the eicosanoids form from the metabolism of EPA is likely the source of the anti-cancer effects seen with these PUFAs. The eicosanoids reduce damage caused by oxidative stress and inhibit the COX-2 inflammatory pathway [2]. EPA and DHA have also been shown to protect tissues that are not the targets of chemotherapy treatment and increase tumor sensitivity to certain cancer treatments [13]. EPA was also shown to increase muscle mass in patients with wasting syndrome, or cachexia, associated with chemotherapy [15]. Though the correlation between increased muscle and body mass and PUFA supplementation may not have been significant in each and every study conducted, overall quality of life was certainly improved in all patients who received supplements [2].

3.2. Algal DHA and Treatment of Cystic Fibrosis Symptoms

Cystic fibrosis is a genetic disease in which mucous membranes, namely in the lung and intestines, do not function properly, causing mucous build-up. Patients with this disease have been found to have lower than normal levels of DHA and arachidonic acid (ARA) in their mucous membrane tissues as well as the blood [3]. This may be due to incomplete digestion of PUFAs as algal DHA supplements appear to be efficiently absorbed by patients with the disease [16]. Lung disease associated with CF is very inflammatory (high levels of ARA) so an increase in DHA derived anti-inflammatory compounds may lead to improvements in lung function by decreasing the ratio between ARA and DHA [3]. Algal DHA is beneficial to CF patients because it manifests fewer gastrointestinal side effects and is more compliant than similar doses of fish oil derived DHA. The doses of algal DHA can also be delivered without increasing pancreatic enzymes doses as well [3]. Algal DHA was found to deliver to red blood cells and plasma at an equal level to fish oils from cooked salmon [11].

3.3. Production of Algal PUFAs

Marine microalgae are a very good source of various PUFAs including EPA, DHA, ARA, and γ-linolenic acid. Certain species and algal strains can be selected for the type and quantities of the PUFAs they produce by manipulating the conditions in which the algae are cultured [6]. Ward and Singh [18] outlined the various species and the compounds they produce in their review of alternate sources of omega 3/6 oils: microalgae of the genera Phaeodatylum and Monodus are good sources of EPA; Schizotrychium species are stable sources of DHA for use in aquaculture, poultry and livestock feeds [19]. One of the problems with algal EPA production is that those species that accumulate EPA in the most available form, triglycerides, are obligate phototrophs, which require expensive photobioreactors for growth [19]. This may be remedied by genetic engineering technology that allows phototrophic species to be converted to heterotrophic species that require much less expensive fermenters for growth and are not hampered by the need for sunlight [18]. Heterotrophic cells can also grow in much higher cell densities compared to phototrophic bacteria because they don’t need sunlight for growth [18].

 

Photobioreactor PBR 4000 G IGV Biotech

A photbioreactor set-up for the cultivation of microalgae
Image source: Wikimedia Commons

 

4. Antibiotic and Antifouling Activity

A study of extracts from Puerto Rican seaweed species showed 64% of the compounds assayed had some level of antibiotic activity [20]. These levels ranged from activity against a single species to activity against the entire range of bacterial species tested. This activity can be contributed to a variety of compounds with the most highly active being brominated compounds in Asparagopsis taxiformis solutions. Though the majority of species tested for antibiotic activity exhibited inhibition against only 1 or 2 microorganisms, 61% of the algae were active against the Gram-positive bacteria Bacilus subtiles and Staphylococcus aureus. Antibiotic activity was evenly distributed against the species in the divisions Rhodophyta, Chlorophyta, and Phaeophyta [20].

Secondary metabolites from marine algae also have activity against bacteria, other algae, fungi, protozoans, and macro species like barnacle larvae. These activities may contribute to algal metabolites making a good source for anti-fouling compounds as all the groups listed above participate in the formation of biofilms on maritime industry properties [1]. Two compounds from the red algae Laurencia rigida, elatol and deschlorelatol, were found to have strong activity against settlement of invertebrate larvae like that of barnacles and oysters [21]. A lactone compound from the brown algae Lobophora variegata, known as lobophorolide, has strong promise as an anti-fungal agent that is environmentally friendly for use in anti-fouling paints [21]. Compounds must meet the standards of the EC Biocide Directive for safety of registered toxins if they are to be used in commercial anti-fouling paints. Isolation of these compounds is very expensive but the solution may lie in genetic engineering. It allows for a safe supply and the potential for development of new compounds to remedy the ever-present problem of biofouling in the maritime industry [1].

5. Carotenoids

Carotenoids are pigment compounds that generally give a yellow, orange, or red color. They are synthesized by plants and algae and may play a role in photosynthesis. These compounds act as antioxidants, reducing stress from oxidative damage. Their bioactivity lies in their physiochemical properties, which depend on the structure of the molecule. Carotenoids also contribute to algae’s nutritive value in feed for aquaculture and animal farming. These values have made algae a potential nutraceutical for human use [7].  Some microalgae of the division Chlorphyta accumulate carotenoids as part of their biomass, including Dunaliella and Haematococcus species [22]. Dunaliella salina is a particularly good natural source of β-carotene, which has been shown to reduce the risk of cancer and degenerative diseases in humans [4, 23].  D. salina is currently being grown for production in open ponds [4, 6]. Haematococcus pluvialisis is one of the richest natural sources of astaxanthin and can be cultivated at a large scale for production of the compound [23]. Lutein is one of the most important carotenoids in foods and for humans. It is used as an additive in aquaculture and poultry operations and may be effective against a variety of disease including cataracts, macular degeneration, and early stages of atherosclerosis [5, 7].  Strains of the green microalga Muriellopsis are the most promising source for algal lutein accumulation and production systems are being developed [7].

Good candidates for algal production of carotenoids will have the same properties as those for production of PUFAs: high cell densities, efficient growth with minimal light, high percentage of desired compounds per cell. Genetic engineering is also an option for carotenoid production but no significant improvements in manipulation of eukaryotic microalgae has been seen so far. Further research and growth studies are required to realize marine algae’s potential for large-scale production [7].

 

D. Salina

[D. Salina.jpg] Natural salt ponds containing Dunaliella salina. The red color is due to their high levels of β-carotene.

6. Biofuels

Most biofuels on the market today are derived from terrestrial sources like oil palms and corn. These biofuels are disadvantageous in that they put a strain on food markets, contribute to water shortages by taking water away from other operations, and further the already rampant destruction of rainforests for resources. Microalgae offer a more economical and environmentally friendly option for the production of biofuels. They have several characteristics that make them more viable biofuel source compared to terrestrial options: they can produce oils year round, they grow in aqueous media and need less water, they can be cultivated on otherwise agriculturally unusable land, and they have a high oil content based on dry mass (20-50%). They may also be able to remove carbon dioxide from the atmosphere and their nitrogen waste may be used as fertilizer [8]. Oil yields may be increased through manipulation of algal growth conditions including temperature, pH, light, carbon dioxide levels, and harvesting methods [6]. Different strains will have the highest oil yield, the highest carbon dioxide fixation rate, the most efficient growth cycle, etc. so strains must be selected for a balance of these traits to create the best overall strains for biofuel production [8].  Once the various strains are produced and a biomass is obtained, the mass must be converted, either thermochemically or biochemically into the usable products for biofuels. There are a variety of conversion methods depending on the starting product and the desired end product [24]. Microalgal production methods are still relatively expensive so further research and engineering are needed in order to choose strains that will be the most effective for biofuel production. The environmentally friendly nature of algae-based fuels is perhaps the most attractive aspect of their use as current options such as palm oil require clear-cutting of rainforests, killing thousands of endangered animals.

7. Conclusions        

Microalgae are a vast, largely untapped resource for a variety of natural products. These products may be used for everything from human health supplements to animal feeds to biofuels. Some of the most valuable compounds derived from marine algae are the polyunsaturated fatty acids, carotenoids, antibiotic compounds, antifungal compounds, antifouling compounds, and oils for biofuels. These compounds may come from macroalgae and microalgae of various divisions including Chlorphyta, Rhodophyta, and Phaeophyta. Though beyond the scope of this review, prokaryotic Cyanobacteria also produce the already listed valuable compounds in addition to some others including neurotoxins.

Further examination of already studied marine algal species and their relatives is necessary for marine algae to truly become one of the great, well-known marine resources. Luckily, they are abundant and offer very little chance for over-exploitation. Their potential for production in an aquaculture setting is also a huge benefit in addition to their valuable secondary actions and products including carbon dioxide fixation and nitrogen waste production for fertilizer. When production becomes more economically feasible and more efficient, marine algae may represent the biggest breakthrough in marine natural product development for medicine and other products.

 

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