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Gloeotrichia cf. natans (Cyanobacteria) in the Continuous Permafrost Zone of Buotama River, Lena Pillars Nature Park, in Yakutia (Russia)

Institute for Biological Problems of Cryolithozone Siberian Branch of Russian Academy of Science (IBPC SB RAS), Lenin av., 41, 677980 Yakutsk, Russia
Polar-Alpine Botanic Garden-Institute—Subdivision of the Federal Research Centre “Kola Science Centre”, 184209 Apatity, Russia
Institute of North Industrial Ecology Problems—Subdivision of the Federal Research Center “Kola Science Center”, 184209 Apatity, Russia
Faculty of Biology and Ecology, Yaroslavl State University, 150057 Yaroslavl, Russia
Papanin Institute for Biology of Inland Waters Russian Academy of Sciences (IBIW RAS), Borok, Nekouz District, 152742 Yaroslavl, Russia
Scientific Research Centre for Ecological Safety, St. Petersburg Federal Research Center, Russian Academy of Sciences, 197110 St. Petersburg, Russia
Institute of Evolution, University of Haifa, Mount Carmel, 199 Abba Khoushi Ave., Haifa 3498838, Israel
Author to whom correspondence should be addressed.
Water 2023, 15(13), 2370;
Submission received: 25 May 2023 / Revised: 20 June 2023 / Accepted: 25 June 2023 / Published: 27 June 2023
(This article belongs to the Special Issue Advances and Challenges of Lake Biodiversity)


As global climate change continues and the vegetation period lengthens, the importance of research into cyanobacterial recruitment biomass and associated toxin risks is growing. While most studies focus on planktonic cyanobacteria causing blooms, benthic cyanobacteria have been less explored. This study reports for the first time on the mass proliferation of benthic epilithic macrocolonies of cyanobacteria, Gloeotrichia cf. natans, in water bodies located in a region with continuous permafrost in Yakutia, North-East Russia. The study characterizes the environmental conditions of its habitat, including the chemical composition of the water, which expands our understanding of this species’ ecology. Cyanotoxins (microcystins, cylindrospermopsin, saxitoxins, and anatoxin-a) were not detected in the biomass of Gloeotrichia cf. natans using liquid chromatography–mass spectrometry and PCR methods.

1. Introduction

Cyanobacteria are an important component of aquatic ecosystems, especially as nitrogen-fixing organisms [1]. However, since many species of cyanobacteria can produce toxins (including hepatotoxins, neurotoxins, cytotoxins, and dermatotoxins), their mass proliferation poses a serious threat to fishing and recreational water use [2,3]. The phenomenon of a rapid increase in planktonic cyanobacteria populations, known as ‘blooms’, has long been the focus of many studies. While research on the mass proliferation of benthic cyanobacteria lags somewhat behind, the associated risks remain insufficiently studied. The number of publications dedicated to the investigation of toxic benthic cyanobacterial species has increased in recent decades, but, despite this, benthic cyanobacteria remain much less studied than planktonic ones [4,5]. Over the past few decades, aquatic ecosystems around the world have become increasingly vulnerable to the effects of phenomena related to global climate change [6,7]. The problem of invasive species, which are colonizing new ecological spaces made available by changes in a number of environmental parameters, has become acute [8]. Invasive taxons, appearing where they were not previously observed, can rapidly grow, and form dominant assemblages, displacing native species [9].
A population of tapering, heterocyte-bearing trichomes arranged radially inside hemispherical or spherical mucilage colonies was recently discovered on a bank of the Buotama River, Yakutia Republic, Russia. It was completely consistent with the description of Gloeotrichia by J. Komárek [10].
In this study, we report for the first time on the mass proliferation of macrocolonies of cyanobacterium Gloeotrichia cf. natans Rabenh. ex Born. et Flah. in the continuous permafrost zone of Yakutia.
According to recent studies [5,11,12,13,14], Gloeotrichia species are known to produce microcystin-LR and microcystin-RR of a potent heptapeptide hepatotoxins group. The Gloeotrichia genus (Aphanizomenonaceae, Nostocales) includes 26 species of filamentous, nitrogen-fixing cyanobacteria that form large colonies [15,16]. Cantoral Uriza et al. [14] report on the toxigenicity of G. natans. The authors conducted extensive sampling throughout Spain under various conditions and in distinct aquatic and terrestrial habitats. Colonies of G. natans were found by the researchers in Lagoa Vixán, Corrubedo, where the species vegetated epiphytically. A strain of G. natans was isolated from the colonies, in which microcystins MC-LF and MC-RR were detected.
The progress of development and distribution of potentially harmful species may have substantial effects on low-nutrient waterbodies used for drinking water handling and recreation. Therefore, we decided to study cyanotoxin production by Gloeotrichia cf. natans colonies.
The aim of this study was to characterize the ecological conditions of Gloeotrichia cf. natans vegetation in the northern river flowing through the continuous permafrost zone, to expand knowledge of the ecology of this species and to test its ability to produce toxins.

2. Materials and Methods

2.1. Study Area

The study area is located in North-East Russia on the 61st parallel north in the continuous permafrost zone. The climate is extremely continental with long, severe winter and short, hot summer. The annual temperature range is of almost 100 degrees: from −60 °C in winter to +40 °C in summer [17]. The region also includes the pole of cold, located in the settlement of Oimyakon, where the lowest temperatures for the Northern Hemisphere have been recorded.
The Buotama River is a right tributary of the middle reaches of the Lena River. The length of the Buotama River is 418 km, and the basin area is 12,600 km2 [18]. The mean annual discharge reaches 43 m3·s−1 [19]. The river is fed by snow and rain. It freezes from October to November, and the ice cover starts to break up from late April to early May [20]. The Buotama River flows through the Lena Pillars National Park, which is a territory under legal protection by an international convention administered by UNESCO and has been inscribed on the World Heritage List. Our research was conducted on the Buotama River, 4 km upstream from its mouth (Figure 1). The width of the river channel at this site is 200 m. The geographic coordinates of the sampling location are 61°13′39.55″ N, 128°46′14.28″ E (WGS 84). The depth of the river channel at a rapid river shoal is 0.3 m, at a reach section of a stream is 2.5 m, and the flow velocity is 0.8 m·s−1 and 0.3 m·s−1, respectively.

2.2. Sampling

Field material was sampled on 16 August 2021. Macrocolonies of Gloeotrichia cf. natans were collected in the lower reaches of the Buotama River on a shallow river shoal and along the riverbanks directly below the shoal. Visible colonies attached to rocks on the pebble at the bottom of the river shoal were detached from the substrate using a plastic spatula. Larger free-floating colonies, which had detached from the substrate and were carried by the current towards the shore, were collected in the immediate vicinity of this river shoal. Macrocolonies were collected in sufficient quantities in this area, from different rocks and various places along the shore, for study under a microscope. This material, in an unfixed, living state, was used for microscopic examination. Another part of this material was immediately frozen at −20 °C for subsequent detection of toxins, PCR analysis and DNA extraction. A water sample for hydrochemical analysis was collected by scooping 2 L and sent to the laboratory for immediate analysis.

2.3. Algological Analysis

Fragments of live macrocolonies were examined under an Olympus BH-2 (Olympus, Tokyo, Japan) light microscope at ×100 and ×400 magnifications. Photomicrographs were obtained using a CK-13 digital camera (Lomo-microsystems, Saint Petersburg, Russia). Identification was carried out following J. Komárek [10].

2.4. Water Chemistry Analysis

Chemical analyses were performed on the water sample using standard methods [21]. Water temperature was measured with an electronic thermometer Chektemp (Hanna Instruments, Woonsocket, RI, USA). pH was measured with a pH-meter/ion meter Multitest IPL-101 (LLC NPP “SEMIKO”, Novosibirsk, Russia). The water color was defined using a photometric method with a spectrophotometer PE-5300VI (GK “EKROS”, Saint Petersburg, Russia). The water salinity was calculated as the sum of ions using different methods: turbidimetry for sulphate anions with a spectrophotometer PE-5300VI, flame spectrophotometry for potassium and sodium cations with automatic flame photometer FPA-2-01 (OJSC “Zagorsk Optical and Mechanical Plant”, Sergiev Posad, Russia), mercurimetry for chloride ions, and titration for calcium, magnesium, and bicarbonate ions. The hardness of water was determined by complexometric titrations using eriochrome black T as an indicator. A photometric method with a spectrophotometer, PE-5300VI, was applied to determine nutrients concentrations. Nessler’s reagent, Griess reagent, salicylic acid, and sulfosalicylic acid were used for the measurement of ammonium ion, nitrite ion, nitrate ion, and total iron, respectively; ammonium molybdate were used for the measurement of phosphate ion and silicon (Si-SiO2). A combined reagent composed of ammonium molybdate, and ascorbic acid was used to determine total phosphorus content. The Fluorat-02-2M device (LLC “Lumex-Marketing”, Saint Petersburg, Russia) was used to determine chemical oxygen demand (COD), petrochemicals, and phenols. The concentrations of manganese, nickel, copper, and zinc were determined using electrothermal vapor¬i¬zation with atomic-absorption spectrometer AAnalyst 400 (PerkinElmer Inc., Waltham, MA, USA).
Analytical quality control was ensured by repeatability limit coefficients (R), which correspond to the values listed below: R = 2 (hardness), R = 3 (Ca, HCO3), R = 6 (SO4), R = 8 (Cl), R = 10 (Mg, Na, K), R = 12 (P tot), R = 13 (NH4), R = 14 (NO3, PO4), R = 17 (NO2), R = 18 (Fe tot), R = 21 (color), R = 25 (COD), R =28 (Cu, Ni, Zn), R = 31 (Si, Mn), R = 48 (phenols), R = 55 (petrochemicals), and R = 0.2 (pH). The measurement result (Xmean) was taken as the arithmetic average of double detection (X1, X2), satisfying the following conditions: ( X 1 X 2 ) R for pH; ( X 1 X 2 )   ( R × ( X 1 + X 2 ) 200 for hardness, calcium (Ca), bicarbonates (HCO3), sulfates (SO4), ammonium (NH4), nitrites (NO2), color; ( X 1 X 2 ) 0.01 × R × X m e a n for magnesium (Mg), sodium (Na), potassium (K), chlorides (Cl), nitrates (NO3), silicon (SiO2), total phosphorus (P tot), phosphates (PO4), COD, iron total (Fe tot), petrochemicals, phenols, manganese (Mn), copper (Cu), nickel (Ni), and zinc (Zn).

2.5. Detection of Cyanotoxins by Liquid Chromatography–Mass Spectrometry

To detect cyanotoxins, analytical-grade chemicals were used for the analysis. Methanol (LiChrosolv hypergrade for LC-MS) and acetonitrile (HPLC-grade) were sourced from Merck (Darmstadt, Germany); and formic acid (98–100%) was bought from Fluka Chemika (Buchs, Switzerland). High-quality water (18.2 MΩ cm−1) was produced by the Millipore Direct-Q water-purification system (Bedford, MA, USA). The MC-LR, MC-YR, and MC-RR standards were obtained from Sigma-Aldrich; the [D-Asp3]MC-LR, [D-Asp3]MC-RR, MC-LA, MC-LY, MC-LW, and MC-LF were sourced from Enzo Life sciences, Inc., New York, NY, USA, anatoxin-a fumarate was obtained from Tocris Bioscience (Bristol, UK). Cylindrospermopsin (CYN) and deoxy-CYN were purchased from the National Research Council, Canada, and Novakits, France.
The method of high-performance liquid chromatography to define the cyanotoxins profile involved using high-resolution mass-spectrometry (HPLC-HRMS) (LTQ OrbiTrap, Finnigan, USA).
The sample preparation was performed following Chernova et al. [22], which involved the extraction of cyanotoxins from the lyophilized biomass samples through treatment with 1 mL of 75% methanol under ultrasound exposure.
Analyses were performed using the LC-20 Prominence HPLC system (Shimadzu, Japan) coupled with a Hybrid Ion Trap-Orbitrap Mass Spectrometer—LTQ Orbitrap XL (Thermo Fisher Scientific, San Jose, CA, USA) according to Chernova et al. [22]. To achieve chromatographic separation, a Thermo Hypersil Gold RP C18 column (100 mm × 3 mm, 3 μm) with a Hypersil Gold drop-in guard column (Thermo Fisher Scientific) was used in the regime of gradient elution.
Mass spectrometric analysis was performed using electrospray ionization in the positive ion detection mode. The identification of target compounds was based on the accurate mass measurement of the protonated molecular ions (resolution of 30,000, accuracy within 5 ppm), the fragmentation spectrum of the ions, and the retention times.

2.6. PCR Analysis of Cyanotoxin Biosynthesis Genes

DNA was extracted from the lyophilized cells of Gloeotrichia cf. natans using the silica adsorption and Diatom DNA Prep 200 kit (Isogene Laboratory Ltd., Moscow, Russia), following the manufacturer’s recommendations. The study searched for four genes responsible for synthesizing microcystins, cylindrospermopsin, anatoxin-a, and saxitoxins, which are mcyE, cyrJ, anaC, and stxA, respectively. Polymerase chain reactions (PCRs) were performed with DreamTaq PCR Master Mix (Thermo Scientific, USA) in a CFX96 Touch thermal cycler (Bio-Rad, Hercules, CA, USA) using specific primers HEP (size of the PCR products 472 bp), cynsulF/cylnamR (584 bp), anaC–genF/anaC–genR (366 bp), and sxtaf/sxtar (600 bp) under amplification conditions given in [23,24,25,26]. Amplicons were separated in 1.5% agarose gel, stained with EtBr, and visualized under UV using a Gel Doc XR+ (Bio-Rad, USA).

2.7. Molecular Approach to Species Identification

The morphological identification of the gathered specimen was supported from molecular phylogenetic evidence with analysis of relation and similarity of 16S rRNA gene sequence. DNA was extracted from the environmental sample with the DNeasy Plant Mini Kit (Qiagen, Hilden, Germany). The amplification of partial 16S rRNA gene and 16S-23S ITS rRNA region was performed using a pair of primers suggested by Wilmotte et al. [27] (1: 5′-CTC TGT GTG CCT AGG TAT CC-3′) and Nübel et al. [28] (2: 5′-GGG GGA TTT TCC GCA ATG GG-3′). PCR was carried out in 20 µL volumes with MasDDTaqMIX (Dialat Ltd., Moscow, Russia), 10 mol of each oligonucleotide primer, and 1 ng of DNA with the following amplification cycles: 3 min at 94 °C, 40 cycles (30 s at 94 °C, 40 s at 56 °C, and 60 s at 72 °C) and a final extension time of 2 min at 72 °C. Amplified fragments were visualized on 1% agarose TAE (mixture of Tris base, acetic acid, and EDTA) gels by ethidium bromide staining, purified using the QIAquick Gel Extraction Kit (Qiagen, Hilden, Germany), and then used as a template in sequencing reactions with the ABI PRISM® BigDye™Terminator v. 3.1 (Applied Biosystems, Foster City, CA, USA) Sequencing Ready Reaction Kit following the standard protocol provided for Applied Biosystems 3730 DNA Analyzer (Applied Biosystems, Foster City, CA, USA) in “Genome” Center of EIMB (Moscow, Russia). Additionally, internal primer 3 (5′-CGC TCT ACC AAC TGA GCT A-39′) by [29] was used in the sequencing procedure.

2.8. Molecular Analyses

The sequence data for the tested sample were assembled using BioEdit 7.0.1 [30] and contained 16S rRNA gene and 16S–23S ITS region. To test phylogenetic affinity, we used GenBank [31] and the recently published database CyanoSeq [32] of cyanobacterial 16S rRNA gene (Lefler et al., 2023 [32]) and thorough preliminary analysis was determined in relation to two strains of the genus Gloeotrichia. The GenBank dataset contained 16S rRNA gene sequence data for additional strain of Gloeotrichia, thus, three strains were included in estimation. Unfortunately, the sequence data for toxin-producing species Gloeotrichia natans are absent in public databases, and we have no possibility of robustly comparing our sample. Preliminary analysis allowed determining the nearest relatives, and, in total, 32 accessions containing sequence data of 16S rRNA gene were selected to illustrate phylogenetic affinity of the tested sample. Atlanticothrix silvestris Alvarenga et al. was chosen as an outgroup. The length of the produced alignment consisted of 1411 sites. A maximum likelihood (ML) method with IQ-TREE [33] was implemented to test phylogeny. The ML analysis of the 16S rRNA gene included a search for the best-fit evolutionary model of nucleotide substitutions with the incorporated option ModelFinder [34] and ultrafast bootstrapping [35] with 1000 replicates. The TIM3 + F+I model was selected as the best-fit evolutionary model with four rate categories of gamma distribution to evaluate the rate of heterogeneity among sites. The similarity of the 16S rRNA gene region of the tested sample was calculated as the average pairwise p-distances in Mega 11 [36,37] using the pairwise deletion option for counting gaps with the following formula: 100 ∗ (1 − p).

3. Results

3.1. Water Chemistry

The water temperature during the sampling event was 17 °C. Water pH was slightly alkaline (Table 1). The water of the river was fresh, with low salinity. In the major ionic composition, the predominance of bicarbonates was detected (32–36%-equiv.). The concentration of chlorides and sulfates was negligible. A large proportion of calcium (45–48%-equiv) was in the cation composition. According to major ionic constituents, the water belonged to the hydrocarbonate class, the calcium group, type 2–3, and hardness was low. The detected concentrations of petrochemicals and phenols were negligible. Concentrations of total phosphorus and mineral phosphorus were low, below the detection limit of the analysis. The content of ammonium nitrogen, nitrate nitrogen, silica, total iron, and nickel were characterized by low values. Slightly elevated indices were noted for COD, water-color index, nitrite nitrogen, manganese, and zinc. The relatively high concentration of copper is of natural origin and has been often noted for the rivers of the studied region [38].

3.2. Field Algological Observations

For the first time, the occurrence of mass growing of cyanobacterial macrocolonies in the estuary of the Buotama River was discovered by us on 5 August 2021. By the term “mass growing”, we mean that cyanobacterial macrocolonies were found on all the stones randomly lifted from the river bottom. (Figure 2c). Large olive–green–brown colonies of irregular spherical shape, hollow inside, with a diameter of 1 to 3 cm, were found lying freely in masses among the pebbles along the river banks (Figure 2a,d). Further investigation revealed cyanobacterial colonies of the same color, of irregular semi-spherical shape, and ranging in size from 1 to 10 mm, were mass growing (Figure 2b) on the bottom of a nearby shallow (up to 0.7 m) river rapids shoal, attached to a pebble substrate. All colonies were dense, slimy to the touch, soft, and mashed when squeezed. The colonies emitted a distinctive earthy odor.
Following the discovery, a field excursion was commenced on 16 August 2021, to gather algological and hydrochemical samples from the field and transfer them to the laboratory.

3.3. Microscopic Survey

Small young colonies of Gloeotrichia cf. natans are initially attached to pebbles underwater onto a river bottom, and later become free-floating and washed onto the river bank. The colonies are composed of densely radially arranged filaments with bases oriented in the center of a colony and embedded in a mucilage matrix (Figure 2e). The colonial slime is firm with periderm and delimited. Sheaths are vase-like, colorless to yellowish, thin, widened at the base, and distant from the trichomes. They are scarcely transversely constricted (Figure 2f,g, denoted with blue arrows). Trichomes have constricted cross-walls at the base and are not constricted away from a base (Figure 2h, denoted with green arrows). Trichomes are heteropolar with a widened base and other ends of the trichomes are elongated into long, cellular hairs. Young cells are cylindrical, longer than wide, later barrel-shaped at the base of trichomes, and slightly shorter than wide up to isodiametric. Cells are olive–green without aerotopes, 5–6 µm wide at the base. Heterocytes are basal, single, and spherical (Figure 2f–h, denoted with black arrows). Akinetes are cylindrical with rounded ends (Figure 2g, denoted with white arrow), straight, or arcuated (Figure 2e, denoted with red arrows), 30–50 × 6–8 µm. Although our specimen morphologically coincided with Gloeotrichia natans, this species is a variable with numerous forms and its robust identification should be confirmed genetically.

3.4. Phylogeny

The identification of cyanobacteria is challenging due to their high morphological variability. The nucleotide sequence of the 16S rRNA gene and the 16S–23S ITS rRNA region for the tested sample was assembled and deposited in GenBank with accession number OR088422. Obtained 16S rRNA gene of Buotama river environmental sample was assessed as having Nostocales-type strains of cyanobacterial CyanoSeq database sequences [32]. The ML analysis of the 16S rRNA gene dataset resulted in a single tree with an arithmetic mean of log likelihood −5549.930; obtained tree topology is shown on Figure 3.
The sample from Buotama River was found in sister relation to the clade composed by three strains of the genus Gloeotrichia with bootstrap support 93%, but it formed a long separate branch. The p-distance estimation (Table 2) showed 99.71–99.86% similarity of 16S rRNA gene among three downloaded strains that lied in infraspecific threshold (<1.3%) for cyanobacteria [37]. The tested sample of Gloeotrichia revealed only 97.54–97.69% similarity to all of them and could be suggested as a distinct species of the genus Gloeotrichia.
Since there are no data on the nucleotide sequence of the 16S rRNA gene of Gloeotrichia natans, we could only rely on correspondence of morphological features of the studied sample to the original morphological description of Gloeotrichia natans and attend gathered sample to this species.
In the future we are going to conduct a study to definitively establish this particular sample’s species classification. Perhaps, we will be able to acquire herbarium data specific to Gloeotrichia natans.

3.5. Cyanotoxins Detection

No anatoxin-a, cylindrospermopsin, or any variants of microcystins were detected in the biomass of Gloeotrichia cf. natans above the detection limit of 0.1 mkg g−1. Furthermore, the absence of the ability of Gloeotrichia cf. natans to produce cyanobacterial hepatotoxins and neurotoxins was confirmed and supplemented by the negative results of PCR amplification of mcyE, anaC, cyrJ, and sxtA genes, which is consistent with the LC/MS data.

4. Discussion

Gloeotrichia natans is a freshwater cyanobacterium that is widely distributed across different regions of the world (Figure 4). Most of the occurrences are in warm climate regions and temperate zones. The exceptions are locations in Komi Republic [39] and the mouth of the Lena River [40].
Occurrences of Gloeotrichia natans have been recorded in Yakutia previously. The discovery of this species in Central Yakutia was reported by L. Ye. Komarenko and I. I. Vasilyeva [43] (Lake Tyungulu) and L. Kopyrina et al. [44] (Lake Dyiere) (Figure 4). V. I. Zakharova et al. [45] reported on the findings of Gloeotrichia natans in the Lena and Aldan rivers’ basins, without definite location.
A few records of this species from the Arctic and Subarctic area have been listed in the open-information system on biodiversity “L.” [41,46]. There is an occurrence of Gloeotrichia natans in a lake on the Samoylovsky island in the Lena River Delta [40] and also in an unnamed peat lake in Kamchatka Peninsula [47]. On the territory of Asian Russia, the species is more common in southern areas and was noted in Primorye Region, Khabarovskyi Region, Amurskaya Oblast, and Sakhalinskaya Oblast [48]. It is known that such a large river crossing the continent in the meridional direction, such as the Lena River, is a transit corridor along which microalgae significantly expand their range to the north [49]. The records of G. natans in Yakutia show that it belonged to the area along the Lena River (Figure 4), which, in our opinion, confirms the hypothesis about the transfer of this species from the southern regions to the north along the course of this large river.
As far as we managed to find out, the mass growing of colonies of this species in the continuous permafrost zone was not noted earlier. The occurrence of Gloeotrichia natans in the Buotama River has not been reported previously, therefore, information on when this species appeared here is absent.
To date, most research on cyanobacterial blooms has focused on high-nutrient lakes. Also, Gloeotrichia natans is known to thrive in eutrophic waters. We recorded the cyanobacterium Gloeotrichia cf. natans in the river with low nitrogen and phosphorus concentrations.
The data we obtained indicate high water quality of the Buotama River. According to the classification of the stream’s trophic state suggested by W. K. Dodds [50], the Buotama River is classified as mesotrophic based on its total phosphorus (Ptot) content and oligotrophic based on its total nitrogen (Ntot) content. The main cause of high water quality might be that the river flows through a protected area where the influence of anthropogenic factors on the water ecosystem is excluded.
Despite the oligotrophic rate of the water course in low-nutrients systems, it occasionally exhibited high levels of cyanobacteria.
Over the past few decades, there has been a growing trend of abnormal development of filamentous cyanobacteria in oligotrophic water bodies in various parts of the world where such occurrences were once non-existent. Scientists have documented instances of extensive proliferation of benthic filamentous cyanobacteria in shallow and pristine water bodies with high water quality, despite the absence of eutrophication indicators [51]. Among the reasons for this phenomenon, the increase in water temperature and the lengthening of the vegetation season are cited, which are associated with modern global climate change [51]. It is known that an increase in water temperature stimulates the growth of filamentous cyanobacteria, which form mats and biofilms on the surfaces of submerged objects [52].
Global climate change has led to changes in the ice regime of water bodies in the studied region. From 1980 to 2014, there was an increase in the duration of the ice-free period of various water bodies in Asian Russia, with an average increase of 4.63 to 11 days per decade [53]. The shortening of the ice-free period leads to an extension of the vegetation season in the region’s water bodies. Therefore, the observed phenomenon of massive proliferation of benthic cyanobacteria may be associated with global climate change. In any case, we believe that this phenomenon requires further study and monitoring in the northern water bodies, particularly in the water bodies of Yakutia.
Gloeotrichia natans is commonly found in a variety of aquatic habitats, including lakes, ponds, rivers, and streams. It can grow in a range of environmental conditions. Its typical habitats are stagnant waters, where it usually grows as an epiphyte on water plants [10,43,54,55]. We found Gloeotrichia cf. natans in a river where aquatic plants are absent, and it was developing epilithically. We did not find any published data on findings of this species in lotic environments or epilithic habitats. Thus, our discovery expands knowledge of the ecology of the species.
Cyanobacteria produce a wide range of metabolites. Among them, are non-toxic odorants and highly toxic metabolites—cyanotoxins. The production of geosmin—the odorant, which emits a characteristic earthy smell—was noted organoleptically. According to F. Jüttner and S. B. Watson [56], the detection threshold of geosmin in humans is very low, in a range of 0.006–0.01 μg L−1 in water. Thus, the massive proliferation of the species could affect the quality of recreational waters. It is known that cyanotoxin-producing species are widely distributed in benthic habitats, with benthic anatoxins being recorded in eight countries and benthic microcystins in 10 countries [5]. In the past two decades, several studies have been published confirming the distribution of cyanobacterial blooms and occurrences of toxic metabolites in benthic habitats of polar and subpolar regions [57,58,59,60,61,62]. Our recent studies of plankton in lakes of Yakutia rendered it possible, for the first time in the cryolithozone of northeastern Russia, to detect the presence of the mcyE gene responsible for the biosynthesis of microcystin cyanotoxins, as well as several structural variants of microcystins [63]. This confirms the possibility of cyanobacteria producing toxic metabolites in the region’s harsh climatic conditions, in water bodies located in the continuous permafrost zone.
Hepatotoxins (microcystins and cylindrospermopsins) and neurotoxins (anatoxin-a and saxitoxins), as well as the genes responsible for their synthesis, were not found in the discovered colonies of Gloeotrichia cf. natans. Therefore, the mass proliferation of G. cf. natans in this region is unlikely to create risks for other aquatic inhabitants and does not pose a threat to human health. However, there are some difficulties in understanding the threat of toxic productivity in benthic habitats, rendering it challenging to detect the environmental conditions that promote the proliferation of toxic cyanobacteria, the nature of their temporal dynamics and life cycle, and the effects of environmental variables [5]. We cannot rule out the possibility that other populations of this species will not exhibit toxicity, or that the studied population, through horizontal transfer, will not acquire toxin-producing genes in the future. So, in our opinion, in the context of global climate change and the lengthening of the growing season in Arctic water bodies, such occurrences of mass proliferation of cyanobacterial species should be constantly monitored.

5. Conclusions

This study, for the first time in the water bodies located in the zone of continuous permafrost, revealed the massive proliferation of cyanobacterium macrocolonies—Gloeotrichia cf. natans. Molecular and analytical methods were used to establish that the studied species Gloeotrichia cf. natans did not produce hepatotoxins and neurotoxins, but we were able to expand knowledge about the ecology of the species and its ability to vegetate epilithically in lotic habitats. Our discovery of Gloeotrichia cf. natans is not the first for the region, but it has not been previously recorded in the studied Buotama River. The waters of the Buotama River are characterized by high quality and low trophic status. In recent decades, in different regions of the world, massive proliferation of benthic cyanobacteria has been observed in oligotrophic water bodies, which is partly attributed to global climate change and an increase in the vegetation period. For water bodies in the northern region we studied, the ice-free period has been decreasing over the past several decades, leading to an increase in the length of the vegetation period. Under these conditions, the occurrence of massive proliferation of benthic cyanobacteria should be closely monitored.

Author Contributions

Conceptualization, V.G. and D.D.; methodology, V.G. and D.D.; software, D.D. and A.V.; validation, S.B., E.C. and S.S.; formal analysis, V.G. and S.S.; investigation, V.G. and O.G.; resources, O.G.; data curation, V.G. and D.D.; writing—original draft preparation, V.G., D.D. and A.V.; writing—review and editing, V.G., S.S., E.C., D.D. and S.B.; visualization, Z.Z.; supervision, V.G.; project administration, V.G.; funding acquisition, V.G., D.D., S.S. and E.C. All authors have read and agreed to the published version of the manuscript.


The research was carried out within the state assignment of the Ministry of Science and Higher Education of the Russian Federation (theme number FWRS-2021-0023, reg. number AAAA-A21-121012190038-0), (theme number 121051100099-5), and within the framework of state budgetary theme no. FFZF-2022-0012, RosRid number 122041100086-5. The study of molecular identification of specimen was funded by the Russian Science Foundation, grant number 21-14-00029 ( accessed on 25 May 2023). Molecular genetic studies were performed by S.I. Sidelev in the scientific educational laboratory “Molecular Genetics and Biotechnology” under YarSU’s development program framework for 2030 (number 123042800011-6).

Data Availability Statement

Not applicable.


This work was partly supported by the Israeli Ministry of Aliyah and Integration.

Conflicts of Interest

The authors declare no conflict of interest.


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Figure 1. The study area. View of the sampling site at the Buotama River (a). Map of the study area with a red dot indicating the sampling point and a green line representing the border of the Lena Pillars National Park (b). Geographic location of the study area (red dot), with a red line showing the administrative border of Yakutia and a black dashed line indicating the polar circle (c).
Figure 1. The study area. View of the sampling site at the Buotama River (a). Map of the study area with a red dot indicating the sampling point and a green line representing the border of the Lena Pillars National Park (b). Geographic location of the study area (red dot), with a red line showing the administrative border of Yakutia and a black dashed line indicating the polar circle (c).
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Figure 2. Macrocolonies of Gloeotrichia cf. natans observed with no magnification, lying freely among pebbles on the riverbank (a); colonies attached to rocks underwater (b), and on a rock lifted out of the water (c); olive–green–brown colonies, that are irregularly spherical and hollow, with diameters ranging from 1 to 3 cm, collected along the riverbank among the pebbles (d). Light microscopy of Gloeotrichia natans reveals a part of the colony consisting of densely radially arranged filaments, with straight or arcuated akinetes visible ((e), denoted with red arrows); basal heterocytes that are single and spherical ((fh), denoted with black arrows), cylindrical akinetes with rounded ends (g, denoted with white arrow); vase-like widened sheaths that are colorless to yellowish, thin, widened at the base, distant from the trichomes, and scarcely transversely constricted ((f,g), denoted with blue arrows); trichomes with constricted cross-walls at the base, and not constricted away from the base ((h), denoted with green arrows); and young cells that are cylindrical, longer than wide, and later barrel-shaped at the base of trichomes (h).
Figure 2. Macrocolonies of Gloeotrichia cf. natans observed with no magnification, lying freely among pebbles on the riverbank (a); colonies attached to rocks underwater (b), and on a rock lifted out of the water (c); olive–green–brown colonies, that are irregularly spherical and hollow, with diameters ranging from 1 to 3 cm, collected along the riverbank among the pebbles (d). Light microscopy of Gloeotrichia natans reveals a part of the colony consisting of densely radially arranged filaments, with straight or arcuated akinetes visible ((e), denoted with red arrows); basal heterocytes that are single and spherical ((fh), denoted with black arrows), cylindrical akinetes with rounded ends (g, denoted with white arrow); vase-like widened sheaths that are colorless to yellowish, thin, widened at the base, distant from the trichomes, and scarcely transversely constricted ((f,g), denoted with blue arrows); trichomes with constricted cross-walls at the base, and not constricted away from the base ((h), denoted with green arrows); and young cells that are cylindrical, longer than wide, and later barrel-shaped at the base of trichomes (h).
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Figure 3. Phylogram obtained under the maximum likelihood approach for 33 accessions of nearest relatives to the genus Gloeotrichia based on the 16S rRNA gene with Atlanticothrix silvestris as the outgroup. Bootstrap support values greater than 50% are indicated. The numbers on the tree branches are a percentage of similarity.
Figure 3. Phylogram obtained under the maximum likelihood approach for 33 accessions of nearest relatives to the genus Gloeotrichia based on the 16S rRNA gene with Atlanticothrix silvestris as the outgroup. Bootstrap support values greater than 50% are indicated. The numbers on the tree branches are a percentage of similarity.
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Figure 4. Distribution of Gloeotrichia natans according to information system “L” [41] and [42] data.
Figure 4. Distribution of Gloeotrichia natans according to information system “L” [41] and [42] data.
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Table 1. Mean values with standard deviations for the chemical components of Buotama River water.
Table 1. Mean values with standard deviations for the chemical components of Buotama River water.
VariableMean ValueStandard Deviation
TDS, mg L−1185.761.8385
Hardness, mmol. L−12.400.0141
Ca, mg L−145.690.2687
Mg, mg L−11.460.0566
Na, mg L−11.190.0707
K, mg L−10.580.0283
HCO3, mg L−1109.840.7071
Cl, mg L−114.180.4243
SO4, mg L−112.820.2828
N-NH4, mg L-10.130.0071
N-NO3, mg L−10.030.0071
N-NO2, mg L−10.030.0
Si-SiO2, mg L−12.040.2828
P tot, mg L−1<0.040.0028
PO4, mg L−1<0.020.0028
Color, Pt/Co grad.444.2426
COD, mg O L−120.202.1213
Fe tot, mg L−1<0.050.0028
Petrochemicals, mg L−10.0050.0014
Phenols, mg L−10.00050.0001
Mn, µg L−133.005.6569
Cu, µg L−16.000.7071
Ni, µg L−14.400.7071
Zn, µg L−113.701.1314
Table 2. The value of p-distances for the Gloeotrichia strains, based on nucleotide sequence data of 16S rRNA gene, %.
Table 2. The value of p-distances for the Gloeotrichia strains, based on nucleotide sequence data of 16S rRNA gene, %.
Gloeotrichia cf. natans 215 OR088422 Russia
G. pisum KLL1-9-20 MZ338338 Israel97.69%
G. pisum SL6-1-1 KY296602 USA97.54%99.71%
G. echinulata PYH14 AM230704 Finland97.69%99.86%99.71%
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Gabyshev, V.; Davydov, D.; Vilnet, A.; Sidelev, S.; Chernova, E.; Barinova, S.; Gabysheva, O.; Zhakovskaya, Z. Gloeotrichia cf. natans (Cyanobacteria) in the Continuous Permafrost Zone of Buotama River, Lena Pillars Nature Park, in Yakutia (Russia). Water 2023, 15, 2370.

AMA Style

Gabyshev V, Davydov D, Vilnet A, Sidelev S, Chernova E, Barinova S, Gabysheva O, Zhakovskaya Z. Gloeotrichia cf. natans (Cyanobacteria) in the Continuous Permafrost Zone of Buotama River, Lena Pillars Nature Park, in Yakutia (Russia). Water. 2023; 15(13):2370.

Chicago/Turabian Style

Gabyshev, Viktor, Denis Davydov, Anna Vilnet, Sergey Sidelev, Ekaterina Chernova, Sophia Barinova, Olga Gabysheva, and Zoya Zhakovskaya. 2023. "Gloeotrichia cf. natans (Cyanobacteria) in the Continuous Permafrost Zone of Buotama River, Lena Pillars Nature Park, in Yakutia (Russia)" Water 15, no. 13: 2370.

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