High quality fresh water is critical for environmental sustainability, and is an essential driver of the world’s economy. Degraded water quality has severe implications for aquatic biodiversity, cultural values, drinking water supplies and water-based recreation. One of the consequences of declining water quality is an increase in cyanobacteria. Photosynthetic cyanobacteria are integral parts of many aquatic ecosystems. However, under favourable conditions cyanobacteria can multiply and form blooms. Cyanobacterial blooms (planktonic blooms or benthic proliferations) are aesthetically unpleasant and can have serious environmental impacts. Additionally, some cyanobacterial species produce natural toxins which are a threat to aquatic life as well as human and animal health. Toxic cyanobacterial blooms have been researched for many decades in lakes, and are usually associated with highly degraded systems. Over the past decade, in rivers worldwide, there has also been a reported increase in proliferations of less well-studied benthic cyanobacteria, such as Microcoleus (Figure 1).
Benthic Microcoleus species studied to-date do not fix nitrogen, and form thick brown/black leathery mats that can smother an entire river bottom and stretch for many tens of kilometres (Figure 2). Some produce potent toxins that affect the nervous system. These toxins are responsible for multiple canine deaths worldwide, put human health at risk and disturb river ecosystems. In contrast to typical cyanobacterial blooms in lakes, benthic cyanobacterial proliferations are occurring in rivers traditionally thought of as having high water quality.
To explore how these blooms reach such a high biomass in rivers when nutrient (particularly phosphorus) concentrations are very low, we sampled a transient summertime proliferation throughout its development, until forecasted heavy rainfall signalled its termination. The river sampled had been under routine monitoring for these events, enabling us to capture early Microcoleus mat formation and associated water chemistry data. Gently clearing river cobbles of incipient growth also aided in resetting the clock on mat develop (Figure 2). Using proteogenomics (reconstructing environmental genomes and using these to identify peptides detected by mass spectrometry), we identified the genes and proteins present in the mat communities over a 19-day proliferation event.
By studying these cyanobacteria in their natural habitat, we were able to gain new insights into their coexistence with other bacteria and microbial eukaryotes, and their various mechanisms for acquiring nutrients from the benthic mat environment. Our study shows they possess mechanisms for storing carbon, nitrogen and phosphorus in granules within their cells (cyanophycin and polyphosphate) for periods when needed for cell growth. It also indicates that throughout a proliferation event Microcoleus species can, and do, source nitrogen via urea and nitrate uptake, and use some of the several mechanisms they are equipped with to source both organic and inorganic forms of phosphorus simultaneously. Proteogenomic data indicated that Microcoleus relied partly on organic phosphorus scavenged from the mat community, while heterotrophic Bacteroidetes and Myxococcales recycled biomass from the cyanobacteria, demonstrating how these benthic mats function as complex interacting microbial communities. Results illustrate the various processes used by benthic cyanobacteria to flourish in low nutrient habitats.