Cyanobacterial Harmful Algal Mats (CyanoHAMs) in tropical rivers of central Mexico and their potential risks through toxin production

Abstract

Cyanobacteria inhabiting lotic environments have been poorly studied and characterized in Mexico, despite their potential risks from cyanotoxin production. This article aims to fill this knowledge gap by assessing the importance of benthic cyanobacteria as potential cyanotoxin producers in central Mexican rivers through: (i) the taxonomic identification of cyanobacteria found in these rivers, (ii) the environmental characterization of their habitats, and (iii) testing for the presence of toxin producing genes in the encountered taxa. Additionally, we introduce and discuss the use of the term "CyanoHAMs" for lotic water environments. Populations of cyanobacteria were collected from ten mountain rivers and identified using molecular techniques. Subsequently, these taxa were evaluated for genes producing anatoxins and microcystins via PCR. Through RDA analyses, the collected cyanobacteria were grouped into one of three categories based on their environmental preferences for the following: (1) waters with high ionic concentrations, (2) cold-temperate waters, or (3) waters with high nutrient enrichment. Populations from six locations were identified to genus level: Ancylothrix sp., Cyanoplacoma sp., and Oxynema sp. The latter was found to contain the gene that produces anatoxins and microcystins in siliceous rivers, while Oxynema tested positive for the gene that produces microcystins in calcareous rivers. Our results suggest that eutrophic environments are not necessarily required for toxin-producing cyanobacteria. Our records of Compactonostoc, Oxynema, and Ancylothrix represent the first for Mexico. Four taxa were identified to species level: Wilmottia aff. murrayi, Nostoc tlalocii, Nostoc montejanii, and Dichothrix aff. willei, with only the first testing positive using PCR for anatoxin and microcystin-producing genes in siliceous rivers. Due to the differences between benthic growths with respect to planktonic ones, we propose the adoption of the term Cyanobacterial Harmful Algal Mats (CyanoHAMs) as a more precise descriptor for future studies.

Keywords: Anatoxins; Benthic cyanobacteria; Cyanobacterial Harmful Algal Mats; Microcystins; Polyphasic approach; River growths.

Fig. 1

Study sites with cyanobacterial mats in central and southeastern Mexico. Monte Alegre (MA), Segundo Dinamo of Magdalena river (SD), Iturbide Dam (PI), San Miguel (SM), San Rafael Channel (CSR), Arroyo Monarca (AM), Agua Blanca (AB), Meco (ME), Tambaque (TA), and Carrizal (EC)

Fig. 2

Redundancy Analysis (RDA) of the cyanobacterial mats in rivers from central Mexico. Sites and abbreviations of chemical and physical parameters are listed in Table 1

Fig. 3

Freshwater cyanobacteria mats in Mexico. a Macroscopic colonies of Cyanoplacoma sp., b their mucilaginous colony, and c transversal view of colony. d Habitat of Wilmottia aff. murrayi and e apical filament with calyptra. f Habitat of Ancylothrix sp. and g apical filament with calyptra. h Habitat of Oxynema sp. and i apical filament with calyptra. Scale bar: Figs. c, d, f, and h = 10 cm; Fig. d = 1 cm; Figs. c, e, g, and i = 10 μm

Fig. 4

Freshwater cyanobacteria mats in Mexico. a Macroscopic colonies of Nostoc montejanii, b mucilaginous colony, and c transversal view of colony. d Habitat of Nostoc tlalocii, e mucilaginous colony, and f transversal view of colony. g Habitat of Compactonostoc sp., h mucilaginous colony, and i transversal view of colony. j Mats of Dichothrix aff. Willey, k false branch and heterocyte, and l apical filament and yellow sheath. Scale bar: a, b, g, and k = 10 cm; b, e, and h = 1 cm; c, f, i, and l = 10 μm

Fig. 5

Phylogeny of the cyanobacteria genus Cyanoplacoma. Sequences marked with a black square correspond to the sequences obtained by amplification of the 16S gene in this study

Fig. 6

Phylogeny of the cyanobacteria order Oscillatoriales. Sequences marked with a black square correspond to the sequences obtained by amplification of the 16S gene in this study

Fig. 7

Phylogeny of the cyanobacteria order Nostocales. Sequences marked with a black square correspond to the sequences obtained by amplification of the 16S gene in this study

Fig. 8

Electrophoresis gels showing PCR products for the identification of microcystins. (1) MA-Nostoc tlalocii (2) AM-Cyanoplacoma sp. (3) AB-C. sp. (4) ME- Oxynema sp. (12) SD- C. sp. (16) ME-Dichothrix aff willei. (19) SD-Wilmottia aff. murrayi. (32) PI-Nostoc tlalocii (36) SM-Compactonostoc sp. (38) CSR-Compactonostoc sp. (39) SM- C. sp. (42) EC-Ancylothrix sp. (46) TA-Nostoc montejanii (49) SM-Wilmottia sp. M: molecular marker. CN: negative control. CP: positive control

Fig. 9

Electrophoresis gels showing PCR products for the identification of anatoxins. (1) MA-Nostoc tlalocii (2) AM-Cyanoplacoma sp. (3) AB-C. sp. (4) ME-Oxynema sp. (16) ME-Dichothrix aff. willei. (19) SD-Wilmottia aff. murrayi. (32) PI-Nostoc tlalocii (42) EC-Ancylothrix sp. M: molecular marker. CN: negative control. CP: positive control