Mat Forming Toxic Benthic Cyanobacteria in New Zealand: Species Diversity and Abundance, Cyanotoxin Production and Concentrations

<p>Recent research has shown that toxic cyanobacteria are more widespread in New Zealand water bodies than previously thought. However, that work has largely focused on planktonic species. Toxin production associated with benthic cyanobacteria is less widely understood despite benthic mat-forming cyanobacteria being prevalent throughout New Zealand rivers. Little is known on species responsible for toxin production, their distribution, frequency and factors triggering toxin production. This study is divided into two phases; (1) a phylogeographic study of benthic cyanobacteria from multiple rivers across New Zealand and (2) an in-depth study of spatial and temporal variability of toxic benthic cyanobacteria in two rivers. Benthic cyanobacterial mats were collected from 22 different waterbodies around New Zealand between January 2005 and December 2008 and their anatoxin content determined using liquid chromatography-mass spectrometry. Thirty seven isolates were obtained from these samples and a polyphasic approach was used to identify them. Liquid chromatography-mass spectrometry and targeted PCR were used to determine if the isolates were producing anatoxins and microcystins. Phormidium autumnale was the dominant cyanobacterium within the isolates, although molecular and morphological data indicated the existence of multiple strains within this species. Two isolates of Ph. autumnale produced anatoxin-a and formed their own clade based on partial 16S rRNA gene sequences. These data indicate that benthic Ph. autumnale mats are composed of multiple morphospecies and anatoxin production is dependant on the presence of anatoxin-producing genotypes. Microcystin production was confirmed in a potentially novel isolate, closely related to Planktothrix spp. This species was responsible for the death of a dog in the Waitaki river (South Island, New Zealand). Cyanobacterial abundance, diversity and toxin production were monitored fortnightly in an in-depth study of the Hutt and Wainuiomata rivers (Wellington, New Zealand), over a 12 month period. Environmental parameters were correlated with cyanobacterial abundance and anatoxin production at eight locations along the rivers to elucidate possible causal factors. Cyanobacterial proliferations and associated anatoxin production were spatially and temporally variable across eight different sampling sites. Both river flow and temperature had a significant effect on cyanobacterial abundance. Multiple physicochemical factors including nutrients and periphyton growth appear to be interacting to influence cyanobacterial abundance. The presence and concentration of anatoxin-a and homoanatoxin-a and their degradation products dihydro-anatoxin-a and dihydro-homoanatoxin-a were also highly variable across all sites and over time. Anatoxin concentration did not correlate with any physicochemical parameters. The results of this study have demonstrated that the prevalence of freshwater cyanotoxin-producing benthic cyanobacteria is widespread in New Zealand and that toxin concentration is variable and unpredictable. This research will assist water managers in addressing the complex management issues associated with benthic cyanobacterial proliferations.</p>

Mat Forming Toxic Benthic Cyanobacteria in New Zealand: Species Diversity and Abundance, Cyanotoxin Production and Concentrations

<p>Recent research has shown that toxic cyanobacteria are more widespread in New Zealand water bodies than previously thought. However, that work has largely focused on planktonic species. Toxin production associated with benthic cyanobacteria is less widely understood despite benthic mat-forming cyanobacteria being prevalent throughout New Zealand rivers. Little is known on species responsible for toxin production, their distribution, frequency and factors triggering toxin production. This study is divided into two phases; (1) a phylogeographic study of benthic cyanobacteria from multiple rivers across New Zealand and (2) an in-depth study of spatial and temporal variability of toxic benthic cyanobacteria in two rivers. Benthic cyanobacterial mats were collected from 22 different waterbodies around New Zealand between January 2005 and December 2008 and their anatoxin content determined using liquid chromatography-mass spectrometry. Thirty seven isolates were obtained from these samples and a polyphasic approach was used to identify them. Liquid chromatography-mass spectrometry and targeted PCR were used to determine if the isolates were producing anatoxins and microcystins. Phormidium autumnale was the dominant cyanobacterium within the isolates, although molecular and morphological data indicated the existence of multiple strains within this species. Two isolates of Ph. autumnale produced anatoxin-a and formed their own clade based on partial 16S rRNA gene sequences. These data indicate that benthic Ph. autumnale mats are composed of multiple morphospecies and anatoxin production is dependant on the presence of anatoxin-producing genotypes. Microcystin production was confirmed in a potentially novel isolate, closely related to Planktothrix spp. This species was responsible for the death of a dog in the Waitaki river (South Island, New Zealand). Cyanobacterial abundance, diversity and toxin production were monitored fortnightly in an in-depth study of the Hutt and Wainuiomata rivers (Wellington, New Zealand), over a 12 month period. Environmental parameters were correlated with cyanobacterial abundance and anatoxin production at eight locations along the rivers to elucidate possible causal factors. Cyanobacterial proliferations and associated anatoxin production were spatially and temporally variable across eight different sampling sites. Both river flow and temperature had a significant effect on cyanobacterial abundance. Multiple physicochemical factors including nutrients and periphyton growth appear to be interacting to influence cyanobacterial abundance. The presence and concentration of anatoxin-a and homoanatoxin-a and their degradation products dihydro-anatoxin-a and dihydro-homoanatoxin-a were also highly variable across all sites and over time. Anatoxin concentration did not correlate with any physicochemical parameters. The results of this study have demonstrated that the prevalence of freshwater cyanotoxin-producing benthic cyanobacteria is widespread in New Zealand and that toxin concentration is variable and unpredictable. This research will assist water managers in addressing the complex management issues associated with benthic cyanobacterial proliferations.</p>

Genome Streamlining, Plasticity, and Metabolic Versatility Distinguish Co-occurring Toxic and Nontoxic Cyanobacterial Strains of Microcoleus

Microcoleus autumnalis , and closely related Microcoleus species, compose a geographically widespread group of freshwater benthic cyanobacteria. Canine deaths due to anatoxin-a poisoning, following exposure to toxic proliferations, have been reported globally.

Aligning research and monitoring priorities for benthic cyanobacteria and cyanotoxins : a workshop summary

In 2018, the US Army Engineer Research and Development Center partnered with the US Army Corps of Engineers–Buffalo District, the US Environmental Protection Agency, Bowling Green State University, and the Cawthron Institute to host a workshop focused on benthic and sediment-associated cyanobacteria and cyanotoxins, particularly in the context of harmful algal blooms (HAB). Technical sessions on the ecology of benthic cyanobacteria in lakes and rivers; monitoring of cyanobacteria and cyanotoxins; detection of benthic and sediment-bound cyanotoxins; and the fate, transport, and health risks of cyanobacteria and their associated toxins were presented. Research summaries included the buoyancy and dispersal of benthic freshwater cyanobacteria mats, the fate and quantification of cyanotoxins in lake sediments, and spatial and temporal variation of toxins in streams. In addition, summaries of remote sensing methods, omic techniques, and field sampling techniques were presented. Critical research gaps identified from this workshop include (1) ecology of benthic cyanobacteria, (2) identity, fate, transport, and risk of cyanotoxins produced by benthic cyanobacteria, (3) standardized sampling and analysis protocols, and (4) increased technical cooperation between government, academia, industry, nonprofit organizations, and other stakeholders. Conclusions from this workshop can inform monitoring and management efforts for benthic cyanobacteria and their associated toxins.

Internal Nutrient Loading Controls Macroalgal and Cyanobacterial Succession in a Coastal Lagoon Restored by Managed Realignment of Agricultural Land

Managed realignment (MR) has been increasingly applied as an adaptation strategy to sea level rise in low-lying coastal areas, but the ecological consequences after flooding agricultural land with seawater are not well known. The restored Gyldensteen Coastal Lagoon represents one of the largest MR projects in Europe to date. The area served as agricultural land for about 150 years before being deliberately flooded with seawater in 2014. This study monitored for 5 years the succession of macroalgae and benthic cyanobacteria driven by changing internal nutrient (DIN = NH4+ + NO2– + NO3–, DON = dissolved organic nitrogen, and DIP = PO43–) loadings in the lagoon after flooding. A massive bloom of opportunistic green macroalgae (dominated by Cladophora spp.) occurred during the first year as response to a substantial loading of DIN and DIP from the newly flooded soils. The macroalgal cover was sparse the following years and the species richness increased with lower loading of particularly DIN. A cyanobacterial bloom controlled by declining DIN and steady DIP concentrations in the water dominated the lagoon and covered all solid surfaces 4 years after flooding. Highest macroalgal species richness with dominance of perennial Fucus vesiculosus and Agarophyton vermiculophylla was recorded 5 years after flooding following a temperature-induced stimulation of soil nitrogen transformation, leading to increased water column DON concentrations and DIN:DIP ratios. The lagoon remains therefore at an unstable tipping point where small and random changes in the DIN:DIP ratio control the balance between blooms of benthic cyanobacteria and high macroalgal species richness. Future MR projects involving agricultural land should prepare the soil to prevent algal blooms driven by sustained internal nutrient loading. Particularly P loading should be avoided to minimize the chances for recurrent blooms of benthic cyanobacteria.

Assessment of the Chemical Diversity and Potential Toxicity of Benthic Cyanobacterial Blooms in the Lagoon of Moorea Island (French Polynesia)

In the last decades, an apparent increase in the frequency of benthic cyanobacterial blooms has occurred in coral reefs and tropical lagoons, possibly in part because of global change and anthropogenic activities. In the frame of the survey of marine benthic cyanobacteria proliferating in the lagoon of Moorea Island (French Polynesia), 15 blooms were collected, mainly involving three species—Anabaena sp.1, Lyngbya majuscula and Hydrocoleum majus-B. Their chemical fingerprints, obtained through high performance liquid chromatography combined with UV detection and mass spectrometry (HPLC-UV-MS) analyses, revealed a high extent of species-specificity. The chemical profile of Anabaena sp.1 was characterized by three major cyclic lipopeptides of the laxaphycin family, whereas the one of L. majuscula was characterized by a complex mixture including tiahuramides, trungapeptins and serinol-derived malyngamides. Toxicity screening analyses conducted on these cyanobacterial samples using Artemia salina and mouse neuroblastoma cell-based (CBA-N2a) cytotoxic assays failed to show any toxicity to a degree that would merit risk assessment with regard to public health. However, the apparently increasing presence of blooms of Lyngbya, Hydrocoleum, Anabaena or other benthic cyanobacteria on coral reefs in French Polynesia encourages the implementation of ad hoc monitoring programs for the surveillance of their proliferation and potential assessment of associated hazards.