Focus February 2017 | Volume 125 | Issue 2
Microcystis Rising: Why Phosphorus Reduction Isn’t Enough to Stop CyanoHABs
Background image: © John D. Wehr/Fordham University
Sharon Levy, based in Humboldt County, CA, has covered ecology, evolution, and environmental science since 1993. She is at work on the book The Marsh Builders: Wetlands in the Fight for Clean Water.
Citation: Levy S. 2017. Microcystis rising: why phosphorus reduction isn’t enough to stop cyanoHABs. Environ Health Perspect 125:A34–A39; http://dx.doi.org/10.1289/ehp.125-A34
Published: 1 February 2017
PDF Version (9.8 MB)
Related EHP Article
At Stone Laboratory, Ohio State University’s island research station in western Lake Erie, a series of otherworldly life forms parades across a video monitor. Stars, double-sided combs, a web of green hexagons, triangles merged with translucent rays that form a living mandala: These are the lake’s phytoplankton seen under high magnification. Microcystis, the organism that dominates the harmful algal blooms (HABs) that plague Lake Erie each summer, shows up onscreen as clumps of spherical cells.
For the people who live on Lake Erie’s shores, Microcystis made its presence most acutely known in August 2014, when a bright green patch of bloom-impacted water spread from Maumee Bay along the Ohio shoreline of western Lake Erie. Fueled by an overload of nutrients running off farm fields in the Maumee watershed, the bloom flowed over the water intake for the city of Toledo. Elevated levels of microcystins, liver toxins produced by Microcystis, forced city officials to distribute a “do not drink” advisory for nearly 500,000 residents. Stores ran out of bottled water, and residents fled Toledo.
Even more widespread and longer-lasting Microcystis blooms occurred in Lake Erie in 2011 and 2015 following intense spring rains that washed phosphorus and nitrogen into the lake, although those blooms did not affect drinking water. Any warming in temperature or increase in heavy spring rains in the Great Lakes region would be a recipe for more frequent and larger algal blooms, but of all HAB-forming species Microcystis would likely benefit the most.1,2
Traditional approaches to managing HABs have focused on controlling phosphorus levels in water. However, new insights into Microcystis ecology challenge long-standing ideas about how best to control these particular blooms. Human-generated phosphorus loads do fuel HABs in Lake Erie and elsewhere, but researchers now understand that an excess of another nutrient, nitrogen, shifts the balance in favor of Microcystis rather than other HAB-forming cyanobacteria, diatoms, or green algae.
“Microcystis relies on nitrogen from the watershed,” says Hans Paerl, a microbial ecologist at the University of North Carolina at Chapel Hill. “Many lakes that have Microcystis blooms are receiving increasing loads of nitrogen from synthetic fertilizers, urban runoff, and atmospheric pollution. Nitrogen is the new part of the story.”
Microcystis on Top
Although cyanobacteria are often referred to as “blue-green algae,” they are not, in fact, algae. Similarly, although blooms of Microcystis and other cyanobacteria species may be lumped in with other HABs, they are more properly known as cyanobacterial HABs, or cyanoHABs.
Cyanobacteria are actually far more ancient than algae, having appeared more than 2.5–3 billion years ago.3 They were the first organisms to evolve photosynthesis, and their proliferation and release of great volumes of oxygen are believed to have profoundly changed the chemical makeup of Earth’s atmosphere.3
“Cyanobacteria have been through extreme geochemical and climate changes,” notes Paerl. “Their playbook is very deep. They’ve adapted to many of the extremes we’re seeing in the Anthropocene—excessive nutrient loads, global warming, record droughts, and extremely heavy rainfall events.”
Microcystis has the ability to outcompete other kinds of phytoplankton. It appears immune to predation by the planktonic crustaceans, such as Daphnia, that usually control populations of green algae and diatoms.2 These “grazers” avoid Microcystis cells, perhaps because they are less able to devour the clumps of cells. In experiments, daphnids seem unaffected by microcystins, which are deadly to vertebrates, but grazers may be put off by other chemicals produced by Microcystis, including protease inhibitors that can halt digestion.1
Microcystis is also rejected by zebra mussels, which rapidly spread throughout Lake Erie after they were inadvertently introduced in the 1980s via ballast water. Zebra mussels are filter feeders that devour algae, and by 1996 they had drastically reduced most phytoplankton populations to 20% of their pre-invasion biovolume (the abundance of cells in an amount of water).4 Zebra mussels spit Microcystis cells back into the water undigested, however, thereby conferring a survival advantange to the hardy cyanobacterium.
Other factors that favor dominance by Microcystis include the cells’ ability to inflate their gas vesicles to rise to the surface of turbid water, where there is plenty of light for photosynthesis. If a cell is running low on phosphorus, its gas vesicles collapse, and it sinks to the bottom where it scavenges this nutrient from the sediments.5 Other kinds of phytoplankton lack this ability.
Microcystin toxins act by bonding with protein phosphatase enzymes, especially in liver cells, causing cell damage. The toxins can cause liver and kidney disease in humans who have been exposed through drinking or swimming in contaminated water.1 In some cases people have been poisoned via inhalation of microcystins near a major bloom.1 In 1996, when a bloom of Microcystis poisoned the water supply of a dialysis clinic in Brazil, 56 people died of liver failure.6 Blooms producing microcystins have also caused severe and often fatal poisonings of livestock, pets, and wildlife.
An Initial Focus on Phosphorus
In the 1960s, Lake Erie was choking on excess phosphorus and nitrogen released in poorly treated sewage, industrial waste, and runoff from farm fields and city streets. Diatoms and multiple species of cyanobacteria absorbed the nutrients and flourished; they formed floating mats that shaded underwater plants, inhibiting photosynthesis and causing them to wither away and decompose.7 As algal cells died, they sank to the bottom, where they too decomposed. Decomposition takes up oxygen, and the result of the blooms was a dead zone, a span of water so depleted of oxygen that no fish, and few invertebrates, could survive. This phenomenon, called eutrophication, occurs on every continent except Antarctica.8
Lake ecologists searched for the key nutrient controlling the growth of HAB-forming species. “Building any living organism is like building a house,” explains Steven Wilhelm, a professor of microbial ecology at the University of Tennessee. “A house needs support beams, doors, and windows. Algae need carbon, nitrogen, and phosphorus. If you don’t have enough of one nutrient, the growth of the algal community is constrained.”
By the late 1960s, researchers suspected that phosphorus was the key nutrient in freshwater blooms.9 Later, pioneering experiments led by David Schindler at the Experimental Lakes Area in Canada showed that adding a combination of phosphorus and nitrogen could quickly turn a pristine lake into a green soup, while the addition of carbon showed no effect.10 The blooms in the fertilized lakes Schindler studied were dominated by the cyanobacteria Anabaena and Aphanizomenon. These organisms are capable of converting nitrogen gas to bioavailable ammonia, a process called fixation. Schindler concluded that controlling nitrogen levels in water would not affect the growth of the blooms, since the species involved could take as much nitrogen as they needed out of the air. His work seemed to prove that phosphorus alone was the nutrient of concern.
A ban on phosphate detergents, combined with phosphorus removal programs at wastewater treatment plants, brought a dramatic improvement in Lake Erie’s water quality. In the late 1980s and early 1990s, HABs faded and populations of walleye and other game fish rebounded. But the lake has since slid backward, once again showing signs of chronic nutrient pollution.
An emerging body of research suggests that a failure to control growing loads of both dissolved reactive phosphorus and reactive nitrogen in agricultural and urban runoff has changed the makeup of the HABs that occur there. Microcystis—which lacks the ability to fix nitrogen—was present in the twentieth-century lake but was relatively scarce. Today, however, it dominates HABs not only in Lake Erie but in polluted waters around the world, including Florida’s Lake Okeechobee, the Baltic Sea, Lake Taihu in China, and Lake Ohnuma in Japan.
The first extensive bloom of Microcystis in western Lake Erie occurred in 1995, and major blooms have since become a predictable summertime event.11 Today the nutrient overload primarily comes from agricultural runoff, but urban runoff can also play a role. Both are hard-to-control “non-point” sources of pollution, meaning their release does not come from a specific source, such as a factory. In 2016 the United States and Canada agreed to a new target of a 40% reduction in Lake Erie’s phosphorus loads compared with 2008 levels, aimed at controlling the annual blooms.12 But researchers delving into the ecology of Microcystis now argue that the traditional approach of focusing on managing loads of total phosphorus ignores the shifting ecology of modern lakes and estuaries.
Nitrogen: The New Part of the Story
In the 1970s, water quality managers believed that phosphorus ran off agricultural land only in particulate form, attached to bits of sediment. A shift toward no-till farming has succeeded in reducing soil erosion and the release of particulate phosphorus, but has been accompanied by a dramatic rise in dissolved reactive phosphorus,13 because fertilizer is spread on the surface of the soil without being tilled under.
Nitrogen also plays a critical role, allowing Microcystis to dominate a community of phytoplankton and fueling its production of toxins. The Haber-Bosch process, which uses a catalyst to transform atmospheric nitrogen into bioavailable ammonia, was developed early in the twentieth century. This process enabled mass production of synthetic fertilizers and transformed the global nitrogen cycle.14 Large regions of the world now receive nitrogen loads more than an order of magnitude higher than natural rates.14 Combustion of fossil fuels also creates significant amounts of bioavailable nitrogen, which settles out of the air into watersheds.1
The amount of nitrogen now flowing into many lakes is much greater than it was in the 1970s, when the phosphorus-only paradigm of eutrophication control emerged. In many watersheds, the focus on phosphorus control means that phosphorus levels have stabilized while nitrogen loading continues. The end result is that the balance of nutrients has shifted in many aquatic ecosystems.15 In addition, since the 1960s synthetic nitrogen fertilizers in the United States have been based less on ammonium nitrate and more on urea, an organic nitrogen compound that can upregulate microcystin production.16
Experiments conducted by Justin Chaffin, Stone Laboratory’s research coordinator, have shown that Microcystis blooms begin when the waters are high in nitrogen.17 Toxin production occurs early in a bloom; later on, the massive population of cyanobacteria has taken up all the available nitrogen—there’s not enough left to use in producing microcystins, which are nitrogen-rich peptides.18 But Microcystis is able to maintain high biomass after water levels of nitrogen have been depleted, Chaffin adds, because it is highly competitive for low levels of bioavailable ammonia.
In Lake Erie, the size of each summer’s HAB reflects phosphorus concentrations at the time.13 But high levels of nitrogen favor dominance of those blooms by Microcystis, and the more nitrogen, the more toxin the bloom will produce.18,19 In other words, reducing phosphorus levels in Lake Erie will reduce the size of any HAB but not necessarily the amount of toxin produced by Microcystis cyanoHABs.
Lake Taihu, in China’s rapidly developing Yangtze River Delta, suffers thick blooms of Microcystis from March through November. More than 40 million people live in Taihu’s watershed, and 10 million rely on the lake for their drinking water.15
Thirty years ago the lake was relatively clean, its phytoplankton community dominated by benign diatoms. Today Taihu is highly eutrophic. In 2007 the water supply for the lakeside city of Wuxi, then home to more than 2 million people, was disrupted for a full week because of microcystin contamination.20
In Taihu, the same problems that affect Lake Erie are magnified because a much larger human population is polluting a shallower, warmer body of water.15 Microcystis thrives in these conditions.21 Lake Taihu’s blooms of Microcystis can be intense and at times can cover the entire lake. “It forms a paint-like, iridescent green scum covering the surface,” says Paerl. “It looks like guacamole with a crust.”
That same description has been used in press reports of recent intense Microcystis blooms on Lake Okeechobee in Florida, which receives polluted farm and urban runoff, and on the St. Lucie Estuary, where Okeechobee’s waters were diverted after unusually heavy rains beginning in the winter of 2015–2016.22 In Okeechobee, as well as Lake Erie, the interaction between nutrient pollution, increased precipitation, and warmer temperature seems to favor the proliferation of Microcystis.1,2
Shifts in Strategy
In China, as in the United States and other nations, runoff from farm fields is a major driver of eutrophication. “In the watersheds of both Lake Erie and Taihu, steps are being taken to retain fertilizer on the land,” says Paerl. Strategies include the creation of vegetated buffers at the edge of farm ditches and constructed wetlands that filter nutrients from runoff.
These techniques can capture both nitrogen and phosphorus, but to solve the problem of non-point nutrient pollution, they may have to be deployed on a large scale that would cover a significant fraction of the landscape. In 2005 William Mitsch, who is eminent scholar and director of the Everglades Wetland Research Park, estimated that 22,000 square kilometers of land would need to be restored to wetland in the Mississippi River Basin to remove 40% of the nitrogen flowing to the Gulf of Mexico.23 In Midwest farmlands, he says today, 7–10% of the landscape would need to be restored to wetlands to capture nutrients flowing off the remaining 90–93%.
Davis notes that regulators are beginning to come to grips with the role of nitrogen in eutrophic lakes. Researchers who guide updates to the Great Lakes Water Quality Agreement,24 a pact between the United States and Canada, are preparing a report on the need to increase the understanding of nitrogen pollution and cycling in Erie and the other Great Lakes.
In 2015 the U.S. Environmental Protection Agency published a report on the need to consider both nitrogen and phosphorus in water quality regulations.25 That report noted that a focus on phosphorus control has not resolved problems in many freshwater bodies, that marine habitats are impacted by heavy loads of nitrogen flowing downstream, and that the relationship between bioavailable nitrogen and cyanoHABs is far more complex than was recognized in the 1970s. “The weight of scientific evidence,” the authors concluded, “supports the development of nutrient criteria for both [nitrogen and phosphorus].”25
If the rise of Microcystis highlights the long-ignored role of nitrogen in eutrophication of fresh waters, it also underscores the difficulty of controlling non-point source water pollution, a task currently managed by each state. Multiple scientists and farmers interviewed for this story indicate that the task of managing non-point source pollution is complicated, because many landowners resent government prescriptions as to how they manage their farms—particularly if they are required to take cropland out of production to create vegetated buffer zones or restore wetlands.
Federal programs offer subsidies to farmers who voluntarily create buffer strips or constructed wetlands on their property.26 A recent modeling study by University of Michigan researchers suggests, however, that reaching the goal of a 40% reduction in Lake Erie’s phosphorus load will take more widespread use and strategic placement of nutrient capture strategies.27 At this point, little is known about the patterns of nitrogen cycling in the Lake Erie watershed.
Major cleanup efforts of point sources of pollution have, in many cases, achieved only a short intermission in the ongoing process of eutrophication. Humanity continues to alter nutrient cycles in ways that affect aquatic habitats worldwide. Rescuing lakes and estuaries from non-point source nutrient pollution will be a long, complex struggle—and success will depend on our awareness of such mundane acts as dropping fertilizer onto soil, as well as our understanding of tiny but powerful organisms like Microcystis.
1. Harke M, et al. A review of the global ecology, genomics and biogeography of the toxic cyanobacterium, Microcystis spp. Harmful Algae 54:4–20 (2016), doi: 10.1016/j.hal.2015.12.007.
2. Michalak A, et al. Record-setting algal bloom in Lake Erie caused by agricultural and meteorological trends consistent with expected future conditions. Proc Natl Acad Sci USA 110(16):6448–6452 (2013), doi: 10.1073/pnas.1216006110.
3. Schirrmeister B, et al. Cyanobacteria and the great oxidation event: evidence from genes and fossils. Palaeontology 58(5):769–785 (2015), doi: 10.1111/pala.12178.
4. Steffen MM, et al. Status, causes and controls of cyanobacterial blooms in Lake Erie. J Great Lakes Res 40(2):215–225 (2014), doi: 10.1016/j.jglr.2013.12.012.
6. Azevedo SMFO, et al. Human intoxication by microcystins during renal dialysis treatment in Caruaru-Brazil. Toxicology 181–182:441–446 (2002), doi: 10.1016/S0300-483X(02)00491-2.
7. Allinger LE, Reavie ED. The ecological history of Lake Erie as recorded by the phytoplankton community. J Great Lakes Res 39(3):365–382 (2013), doi: 10.1016/j.jglr.2013.06.014.
9. Edmondson WT. Nutrients and phytoplankton in Lake Washington. In: Nutrients and Eutrophication: The Limiting-Nutrient Controversy. Proceedings of a Symposium Held at the W.K. Kellogg Biological Station, Michigan State University, February 11–12, 1971. Likens GE, ed. Lawrence, KS:American Society of Limnology and Oceanography (1972), 172–193.
10. Schindler DW. Evolution of phosphorus limitation in lakes. Science 195(4275):260–262 (1977), doi: 10.1126/science.195.4275.260.
11. Watson SB, et al. The re-eutrophication of Lake Erie: harmful algal blooms and hypoxia. Harmful Algae 56:44–66 (2016), doi: 10.1016/j.hal.2016.04.010.
12. U.S. EPA. Governments of Canada and the United States Announce Phosphorus Reduction Targets of 40 Percent to Improve Lake Erie Water Quality and Reduce Public Health Risk [press release]. Washington, DC:U.S. Environmental Protection Agency (22 February 2016). Available: https://www.epa.gov/newsreleases/governments-canada-and-united-states-announce-phosphorus-reduction-targets-40-percent [accessed 11 January 2017].
13. Baker D, et al. Phosphorus loading to Lake Erie from the Maumee, Sandusky and Cuyahoga rivers: the importance of bioavailability. J Great Lakes Res 40(3):502–517 (2014), doi: 10.1016/j.jglr.2014.05.001.
14. Galloway J, et al. Transformation of the nitrogen cycle: recent trends, questions and potential solutions. Science 320(5878):889–892 (2008), doi: 10.1126/science.1136674.
15. Paerl H, et al. Controlling cyanobacterial blooms in hypertrophic Lake Taihu, China: will nitrogen reductions cause replacement of non-N2 fixing by N2 fixing taxa? PLoS One 9:e113123 (2014), doi: 10.1371/journal.pone.0113123.
16. Paerl H, et al. It takes two to tango: when and where dual nutrient (N & P) reductions are needed to protect lakes and downstream ecosystems. Environ Sci Technol 50(20):10805–10813 (2016), doi: 10.1021/acs.est.6b02575.
17. Chaffin JD, et al. Nitrogen constrains the growth of late summer cyanobacterial blooms in Lake Erie. Adv Microbiol 3(6A):16–26 (2013), doi: 10.4236/aim.2013.36A003.
18. Gobler CJ, et al. The dual role of nitrogen supply in controlling the growth and toxicity of cyanobacterial blooms. Harmful Algae 54:87–97 (2016), doi: 10.1016/j.hal.2016.01.010.
19. Harke MJ, et al. Nutrient-controlled niche differentiation of western Lake Erie cyanobacterial populations revealed via metatranscriptomic surveys. Environ Sci Technol 50(2):604–615 (2016), doi: 10.1021/acs.est.5b03931.
20. Qin B, et al. A drinking water crisis in Lake Taihu, China: linkage to climatic variability and lake management. Environ Manage 45(1):105–112 (2010), doi: 10.1007/s00267-009-9393-6.
21. Paerl HW, Huisman J. Blooms like it hot. Science 320(5872):57–58 (2008), doi: 10.1126/science.1155398.
22. Henry T. Lake Erie, South Florida Algae Crises Share Common Toxins and Causes. Toledo Blade, Local section, online edition (24 July 2016). Available: http://www.toledoblade.com/local/2016/07/24/Lake-Erie-S-Florida-algae-crises-share-common-toxins-and-causes.html [accessed 11 January 2017].
23. Mitsch WJ, et al. Nitrate-nitrogen retention in wetlands in the Mississippi River basin. Ecol Eng 24(4):267–278 (2005), doi: 10.1016/j.ecoleng.2005.02.005.
24. IJC. Great Lakes Water Quality: Great Lakes Water Quality Agreement [website]. Washington, DC:International Joint Commission (2017). Available: http://www.ijc.org/en_/Great_Lakes_Quality [accessed 11 January 2017].
25. U.S. EPA. Preventing Eutrophication: Scientific Support for Dual Nutrient Control. EPA-820-S-15-001. Washington, DC:U.S. Environmental Protection Agency (February 2015). Available: https://www.epa.gov/sites/production/files/documents/nandpfactsheet.pdf [accessed 11 January 2017].
26. USDA. Western Lake Erie Basin Project [website]. Columbus, OH:Natural Resources Conservation Service Ohio, U.S. Department of Agriculture (undated). Available: https://www.nrcs.usda.gov/wps/portal/nrcs/detail/oh/programs/?cid=nrcs144p2_029640 [accessed 11 January 2017].
27. Scavia D, et al. Informing Lake Erie Agriculture Nutrient Management Via Scenario Evaluation. Ann Arbor, MI:Water Center, Graham Sustainability Institute, University of Michigan (April 2016). Available: http://graham.umich.edu/media/pubs/InformingLakeErieAgricultureNutrientManagementviaScenarioEvaluation.pdf [accessed 11 January 2017].
We are pleased to announce our new impact factor of 9.78, up from 8.44 last year. Based on our impact factor, EHP is now #4 out of 229 Environmental Science journals, #4 out of 176 Public, Environmental & Occupational Health journals, and #2 out of 92 Toxicology journals. Thanks to all the authors, reviewers, readers, and EHP staff who have contributed to our success.
EHP is pleased to announce that it is now operating under a continuous publication workflow! As indicated in a previous announcement, continuous publication allows EHP to post new content online throughout the month, as each paper becomes ready for an issue. This gets content out to our readers much more quickly than the old issue-based model, and unlike our previous Advance Publication model, these are final, edited articles. (more…)