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Review

Recent Advances in the Ecology of Bloom-Forming Raphidiopsis (Cylindrospermopsis) raciborskii: Expansion in China, Intraspecific Heterogeneity and Critical Factors for Invasion

by
Ling Zheng
1,
Yang Liu
2,
Renhui Li
3,
Yiming Yang
4 and
Yongguang Jiang
1,*
1
Department of Biological Sciences and Technology, School of Environmental Studies, China University of Geosciences, Wuhan 430074, China
2
College of Life Sciences, Henan Normal University, Xinxiang 453007, China
3
College of Life and Environmental Sciences, Wenzhou University, Wenzhou 325035, China
4
Guangdong Engineering Research Center of Oral Restoration and Reconstruction, Guangzhou Key Laboratory of Basic and Applied Research of Oral Regenerative Medicine, Affiliated Stomatology Hospital of Guangzhou Medical University, Guangzhou 510182, China
*
Author to whom correspondence should be addressed.
Int. J. Environ. Res. Public Health 2023, 20(3), 1984; https://0-doi-org.brum.beds.ac.uk/10.3390/ijerph20031984
Submission received: 24 November 2022 / Revised: 9 January 2023 / Accepted: 18 January 2023 / Published: 21 January 2023
(This article belongs to the Special Issue Environmental Microbiology and Water Pollution Applications)
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Abstract

:
Water blooms caused by the invasive cyanobacterium Raphidiopsis raciborskii occur in many reservoirs in the tropical and subtropical regions of China. In recent decades, this species has spread rapidly to temperate regions. Phenotypic plasticity and climate warming are thought to promote the worldwide dispersion of R. raciborskii. However, investigations into the genetic and phenotypic diversities of this species have revealed significant intraspecific heterogeneity. In particular, competition between R. raciborskii and Microcystis aeruginosa was highly strain dependent. Although the concept of an ecotype was proposed to explain the heterogeneity of R. raciborskii strains with different geographic origins, microevolution is more reasonable for understanding the coexistence of different phenotypes and genotypes in the same environment. It has been suggested that intraspecific heterogeneity derived from microevolution is a strong driving force for the expansion of R. raciborskii. Additionally, temperature, nutrient fluctuations, and grazer disturbance are critical environmental factors that affect the population establishment of R. raciborskii in new environments. The present review provides new insights into the ecological mechanisms underlying the invasion of R. raciborskii in Chinese freshwater ecosystems.

1. Introduction

Cyanobacterial blooms are severe environmental problems in eutrophic freshwater ecosystems [1,2]. Raphidiopsis raciborskii (previously known as Cylindrospermopsis raciborskii) is a filamentous bloom-forming cyanobacterium belonging to Nostocales with heterocysts and akinetes (Figure 1A). Upon the occurrence of an R. raciborskii bloom, a significant amount of cell filaments usually distributes evenly in the water column (Figure 1B). As a major producer of hepatotoxic cylindrospermopsin (CYN) and its analogs (Figure 1C) [3,4,5,6], R. raciborskii often proliferates in lakes or reservoirs in tropical and subtropical zones [7,8], posing a significant threat to ecological safety. In the past decades, the occurrence frequency of this species has been significantly increased over the world, including both subtropical and temperate zones of the globe [7,9,10]. Therefore, R. raciborskii was suggested to be an invasive cyanobacterium, and much attention has been paid to its dispersion routes and adaptation mechanisms [9,11,12].
Based on the phylogenetic relationship of strains isolated worldwide, three hypotheses have been proposed for the biogeographic origin and global dispersion of R. raciborskii [7]. First, R. raciborskii was suggested to be derived from tropical regions in Africa due to its temperature dependence and the high diversity of African strains [13]. After invasion and colonization in Australia, R. raciborskii was dispersed throughout Eurasia and America [13]. Similarly, a recent study on the biogeography of R. raciborskii supports central Africa as the original dispersion center for nontoxic strains of this species [14]. The ability to produce CYN and paralytic shellfish poison (PSP) is thought to be acquired after dispersion to new settlements in tropical Africa and the South American continent [14]. Second, it was thought that R. raciborskii was extinct in most areas of the world during the Pleistocene Ice Age, except for the warm refuges of each continent at low latitudes [15]. The surviving R. raciborskii strains were dispersed to high-latitude areas when the global climate became warm. Third, R. raciborskii was thought to be derived from a tropical region in America and dispersed to other continents [11]. Considering that phylogeographic analysis was strongly affected by the genetic variation of the strains used in different studies [16], sufficient strains from different continents and environments should be investigated to clarify the dispersion route of R. raciborskii.
The invasion success of R. raciborskii was mainly ascribed to its phenotypic plasticity and growth optimization under different environments [9,17,18,19,20]. R. raciborskii is tolerant to low and high light intensity and a wide range of temperatures [19,21,22,23,24,25]. This species has flexible strategies for utilizing various forms of nitrogen (N), such as accumulating nitrogen as cyanophycin [26] and switching to N2 fixation under N depletion [27,28,29]. With a strong affinity for phosphate, R. raciborskii is capable of absorbing and storing a lot of phosphorus (P) [18,30]. After depletion of inorganic P, dissolved organic phosphorus can be used by R. raciborskii through the secretion of alkaline phosphatase (ALP) [31,32]. Thus, R. raciborskii can be dominant in the phytoplankton community at both very low and high N:P ratios [33]. In addition, it has been suggested that this species has a competitive advantage over other bloom-forming cyanobacteria under N- or P-limited conditions [30,34,35]. For example, toxic R. raciborskii is favored by the allelopathic effects of CYN on the surrounding phytoplankton [36,37,38,39].
Recent investigations have revealed high genetic and phenotypic diversity within the population of R. raciborskii [40,41,42]. The adaptation mechanisms of different strains were divergent and the competitive advantage of R. raciborskii against Microcystis aeruginosa was strain dependent [43,44,45,46]. These findings indicated apparent intraspecific heterogeneity in R. raciborskii. A comprehensive investigation of R. raciborskii diversity and dispersion in local ecosystems can provide new insights into its invasion success. R. raciborskii has been detected in many lakes and reservoirs in China [8,35,47,48,49,50,51,52]. The recent expansion of R. raciborskii in Chinese freshwater bodies, its intraspecific heterogeneity, and critical factors for its invasion are the focus of this review.

2. Distribution and Dispersion in China

The first reported R. raciborskii bloom in Chinese water bodies occurred in 2002 at 21°59′ N–22°25′ N and 113°05′ E–113°25′ E [53]. To date, the presence of this species has been observed from 20°09′ N to 39°59′ N and between 100°03′ E and 121°41′ E, that is, from the tropical to temperate regions of China (Table S1, Figure 2). R. raciborskii was distributed in the basins of Zhujiang River, Yangtze River, Huaihe River, Yellow River, Haihe River, Yongjiang River, Qiantang River, and in the southeastern rivers in Fujian and Taiwan (Figure 2). Dominance or high biomass of this species was observed in most of the basins, except in the Haihe and Qiantang River basins. The Haihe River basin is the northernmost line with the presence of R. raciborskii in China [50]; this species may have dispersed to this basin recently and has not been fully adapted to the local environment. Given that the Qiantang River basin is located in a subtropical zone with favorable temperature conditions for the proliferation of R. raciborskii, its distribution in this basin needs further investigation. Although historical data on R. raciborskii distribution are lacking, it should be noted that bloom events of this species have increased in recent decades. In 2006, only a low concentration of R. raciborskii filaments was observed in Liangzi lake (30°10′ N, 114°36′ N) [48]. However, its biomass reached 52.03 mg L−1, with an obvious water bloom between 2013 and 2017 [35]. This finding indicates that R. raciborskii has evolved from an occasional species to a dominant species in Liangzi lake, which is likely a typical succession process after the invasion of new water bodies.
The wide distribution of R. raciborskii in the same basin (Figure 2) indicated that this species might be dispersed from upstream lakes to downstream lakes through the river (Figure 3). On the other hand, lakes located separately in floodplain could be linked by large floods, creating opportunities for R. raciborskii to invade new environments. Water diversion projects (WDPs) also provide an important dispersion route for aquatic organisms. For example, fish invasion has occurred through the south-to-north WDP in China [54]. This WDP is designed to divert water from humid subtropical areas to arid or semi-arid temperate areas and thus is favorable for the dispersion of R. raciborskii. Five lakes in the Huaihe River basin were linked with three reservoirs and one pond in the Yellow and Haihe River basins by the east route of the south-to-north WDP (Table S1), and abundant R. raciborskii were observed in all of these water bodies. In addition, the filaments of this species can be conveyed between lakes via natural water used for the transport of aquatic products and ballast water of commercial ships [7]. Owing to their high survivability, the akinetes of R. raciborskii are likely to be transported by migratory birds via feet or gut carryover [55].
CYN is synthesized by a series of enzymes encoded by cyr genes [56]. Characterizing the distribution and variation of cyr genes can provide insights into the dispersion of CYN-producing R. raciborskii strains. A systematic investigation into the sequences of cyrI and cyrJ genes in Chinese water bodies divided them into four and three main sequence types, respectively (Table 1) [48]. It was shown that low-latitude reservoirs contain more sequence types. Given that Itype4af and Itype4ar are Itype1 variants with transposition elements, and that Jtype2b is a Jtype2a variant with a deletion of six nucleotides, the Tiegang reservoir presumably contains all the ancestral cyrI and cyrJ sequence types. This finding indicated that low-latitude lakes in Southeast China are potential dispersion centers of toxic R. raciborskii. Similarly, the tropical regions in Southeast China were also thought to be a glacial refuge for higher plant species [57]. These findings provide further evidence for the refuge hypothesis about R. raciborskii dispersion [15]. PSP-producing R. raciborskii strains were also isolated and identified from Chinese water bodies [58,59]. Phylogenetic analysis revealed that these strains were closely related to strains from the North and South American continents [58]. This finding may imply the dispersion of PSP-producing strains from America to China because the ability of R. raciborskii to produce PSP was proposed to originate from America [14].

3. Intraspecific Heterogeneity

3.1. Phenotypic and Genetic Diversity

In previous studies on the environmental adaptability of R. raciborskii, it has often been regarded as a homogenous population because of the highly similar 16S rRNA genes of different strains. For example, most present studies suggest that R. raciborskii is a mesophile with a tolerance to low temperatures [7,19,60,61]. However, laboratory experimentation has found that several strains maintain a high growth rate at 15 °C, while the growth of some strains is completely inhibited under low-temperature conditions [17,47]. These findings indicate that low-temperature tolerance is not an intrinsic characteristic of R. raciborskii and that significant intraspecific heterogeneity exists for the temperature adaptability of this species. Similarly, the intraspecific heterogeneity of R. raciborskii has also been found in its response to light intensity [9,62,63] and conductivity [64], as well as its strategies for the utilization of N [26,27] and P [41]. In addition, varied growth rates, morphologies, and toxicities have been observed in genetically similar isolates of R. raciborskii [65,66].
In contrast to the 16S rRNA gene, the RNA polymerase C1 (rpoC1) gene and ITS-L sequence, which is the larger fragment of the inter-transcribed sequence of rRNA, are useful molecular markers for discriminating different R. raciborskii strains [58,67]. The strains were classified into nontoxic, CYN-producing, and PSP-producing clusters based on the phylogenetic analysis of rpoC1 and ITS-L [58]. This result is supported by the genomic variations between R. raciborskii strains [16,42,68]. The relationship between genetic diversity and phenotypic variation remains to be clarified and requires further systematic investigation.
The presence of cyr genes is the main genetic difference between CYN-producing and non-CYN-producing strains [48]. However, genomic variations were also found in genes associated with stress and adaptation, which are probably related to the physiological role of CYN [42]. In fact, CYN has been shown to contribute to the successful invasion and survival of R. raciborskii [4,5]. For example, CYN-producing strains have a competitive advantage under nutrient-replete conditions [69]. In comparison to nontoxic R. raciborskii, toxic strains have a more efficient response to inorganic phosphorus and could become dominant in the community [70]. A recent study also found that toxic strains were more competitive under Fe-starved conditions [71].
Previous investigations have revealed that the cell quotas of CYN varied significantly between R. raciborskii strains [65,66,72]. However, the genetic basis of this finding remains unknown. As aforementioned, sequence variations were observed for cyrI and cyrJ genes, which encodes a hydroxylase and a sulfotransferase, respectively [48,73,74,75]. These two enzymes catalyze tailoring reactions in the last two steps of CYN biosynthesis [56]. An inactivated mutation of cyrI inhibits the synthesis of CYN, leading to an accumulation in the intermediate product 7-deoxy-CYN [76]. Therefore, variations in cyr genes may change the activity of the enzymes encoded by them and further affect CYN synthesis efficiency.

3.2. Competition between R. raciborskii and M. aeruginosa

M. aeruginosa is the dominant species in most eutrophic water bodies, both in China and worldwide [51,77]. Competition against M. aeruginosa is inevitable for R. raciborskii during invasion. However, recent culture experiments have produced inconsistent results regarding the competition between R. raciborskii and M. aeruginosa (Table 2). Under light- or P-limited conditions, both R. raciborskii and M. aeruginosa are likely to dominate the mixed culture of these two species with equal starting biovolumes [45]. R. raciborskii, with N-fixation capability, was a more successful invader than M. aeruginosa when N was depleted in batch culture [35]. Likewise, the model prediction of species competition outcomes is strongly affected by the growth variability of strains [78]. These findings demonstrate the intraspecific heterogeneity for R. raciborskii and M. aeruginosa [44].

3.3. Ecotype and Microevolution

In several studies, R. raciborskii was assumed to have evolved into different ecotypes with special physiological characteristics in its original habitats, and the geographic dispersion of this species is a dynamic selection process for existing ecotypes [60,61,72]. The concept of an ecotype is reasonable for understanding the intraspecific heterogeneity of R. raciborskii in different environments but not for explaining the coexistence of different phenotypes and genotypes in the same environment [16,65]. Heterogeneity between coexisting strains is better defined as microevolution, the concept of which refers to minor variations within species [80]. Microevolution is the source of adaptive variation for organisms, and the accumulation of microevolution may further lead to new speciation. The ecotypes of R. raciborskii were presumably established by the natural selection of heterogeneous strains generated during microevolution.

4. Critical Factors for Invasion

4.1. Temperature and Effective Accumulated Temperature (EAT)

Temperature is an important ecological factor that drives the global distribution of R. raciborskii [10,13,81]. Climate warming is expected to increase the biomass of this species and promote its dispersion in new habitats (Table 3). In addition to its proliferation in warm areas, the dominance and bloom of this species were observed in cool water between 10 °C and 15 °C [22,47]. This finding indicates that R. raciborskii is likely to disperse and survive in most freshwater bodies in China. Under nutrient-replete conditions, the potential biomass that R. raciborskii can reach is probably determined by the Effective Accumulated Temperature (EAT) affecting the heat that organisms can obtain during multiplication seasons. To date, there are no available data on the effects of EAT on the growth of R. raciborskii. In China, the EAT varies with latitude from south to north and altitude from east to west. It is necessary to investigate the relationship between EAT and the distribution of R. raciborskii to assess the bloom risk this species presents.

4.2. Nutrient Fluctuations

The coexistence of multiple species is frequently observed during cyanobacterial blooms in eutrophic water bodies [51]. This finding implies that competitive exclusion does not occur, which may be attributed to nutrient repletion in the environment. For example, R. raciborskii may invade into an M. aeruginosa-dominated culture and survive with relatively low biomass [35]. The coexistence of R. raciborskii and M. aeruginosa has been found in many subtropical water bodies located in the Yangtze River basin [35]. Sometimes, R. raciborskii becomes the dominant species in the phytoplankton community. Considering intraspecific heterogeneity, it cannot be predicted that R. raciborskii will eventually compete against M. aeruginosa.
Niche and fitness differences are thought to determine invasion success in bacterial communities [82]. Field investigations have demonstrated that Raphidiopsis, rather than Microcystis, benefit from low P concentrations [83]. This finding was supported by laboratory experiments indicating that R. raciborskii could be advantageous under P-limited conditions [34,84]. This advantage may be enhanced using the allelopathic effects of CYN, which can induce extracellular ALP production in other phytoplankton species [39,85]. In addition, stoichiometric analysis revealed a lower metabolic cost of synthesizing CYN than that of producing ALP [39]. Moreover, N limitation may favor the growth of R. raciborskii strains with N-fixation capability. However, previous studies have claimed that this high-energy-consuming function cannot support the proliferation of R. raciborskii [40]. Nutrient fluctuations frequently occur in natural water bodies [84,86,87]. Intermittent P and N limitations may create opportunities for R. raciborskii to become dominant in the phytoplankton community [87] and proliferate when nutrients are repleted (Table 3).

4.3. Grazer Disturbance

Local grazers have a significant impact on the structure of phytoplankton communities [88]. Daphnia feeding on R. raciborskii can hamper the population establishment of this species [88,89], whereas copepods, preferentially grazing on non-Raphidiopsis species, can promote the persistence of R. raciborskii [90,91] (Table 3). Therefore, a low grazing pressure or loss of top-down control is a critical factor for the invasion success of R. raciborskii [88]. In addition, CYN-producing strains may be more advantageous because of the toxicity of CYN on zooplankton [5].

5. Conclusions

R. raciborskii has spread widely in Chinese freshwater bodies in recent decades. In addition to its adaptability to various environments, the intraspecific heterogeneity of R. raciborskii presumably has a significant contribution to the species’ rapid expansion. Temperature, nutrient fluctuations, and grazer disturbance are important factors that affect the invasion success of R. raciborskii.

6. Perspectives

6.1. Hypothesis for the Invasion Success of R. raciborskii

Field populations of R. raciborskii are mixtures of heterogeneous strains. When the mixtures were dispersed in new environments, strains with strong adaptability could survive under natural selection and evolve into ecotypes with specific genetic and phenotypic characteristics. Some ecotypes of R. raciborskii are likely to proliferate and form blooms under appropriate conditions. In summary, the invasion success of R. raciborskii may be ascribed to sufficient intraspecific heterogeneity, rather than the adaptability of individual strains.

6.2. Future Outlook

Given that R. raciborskii has a growth advantage under nutrient-limited conditions, the expansion of this species may benefit from a reduction in P and N during the remediation of lake eutrophication [92]. To enhance our understanding of the bloom-forming mechanisms of R. raciborskii, knowledge of the intraspecific heterogeneity of R. raciborskii should be strengthened in the future. To accurately discriminate between strain differences, quantitative traits should be defined and investigated systematically. The growth rate, photosynthetic rate, electron transfer rate, affinity for inorganic carbon, pigment content, extracellular ALP activity, toxin content, and critical requirements for nutrients, temperature, and light intensity, are candidate quantitative traits for R. raciborskii. Moreover, highly variable genetic markers, such as ITS-L, can be used to discriminate strain differences at the molecular level. The consistency between molecular markers and quantitative traits should be carefully evaluated. Moreover, it is crucial to identify genes controlling quantitative traits to provide more reliable genetic evidence for the heterogeneity of R. raciborskii.
When a specific field population of R. raciborskii is investigated, many strains should be isolated to fully capture their variability. Considering the effects of in-culture evolution on laboratory experiments [93], strains should be maintained under conditions similar to their original habitats, and their quantitative traits should be characterized after isolation as soon as possible. To develop a worldwide database describing the intraspecific heterogeneity of R. raciborskii, unified and standard experimental methods and procedures are required. Furthermore, attention should be paid to the effects of EAT on the distribution and heterogeneity of R. raciborskii for assessing its bloom risk.

Supplementary Materials

The following supporting information can be downloaded at: https://0-www-mdpi-com.brum.beds.ac.uk/article/10.3390/ijerph20031984/s1, Table S1: Distribution of Raphidiopsis raciborskii in Chinese freshwater bodies. References [8,35,47,48,50,52,53,69,83,85,92,94,95,96,97,98,99,100,101,102,103,104,105,106,107,108] are cited in the supplementary materials.

Author Contributions

L.Z.: investigation, validation, and data curation. Y.L.: validation and writing—review and editing. R.L.: validation and writing—review and editing. Y.Y.: investigation and data curation. Y.J.: funding acquisition, conceptualization, and writing—original draft. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China, grant number 31170189 and 31901185; China Postdoctoral Science Foundation, grant number 2015M572349.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Huisman, J.; Codd, G.A.; Paerl, H.W.; Ibelings, B.W.; Verspagen, J.M.H.; Visser, P.M. Cyanobacterial blooms. Nat. Rev. Microbiol. 2018, 16, 471–483. [Google Scholar] [CrossRef] [PubMed]
  2. Ho, J.C.; Michalak, A.M.; Pahlevan, N. Widespread global increase in intense lake phytoplankton blooms since the 1980s. Nature 2019, 574, 667–670. [Google Scholar] [CrossRef] [PubMed]
  3. La Cruz, A.A.D.; Hiskia, A.; Kaloudis, T.; Chernoff, N.; Hill, D.; Antoniou, M.G.; He, X.; Loftin, K.A.; Oshea, K.E.; Zhao, C. A review on cylindrospermopsin: The global occurrence, detection, toxicity and degradation of a potent cyanotoxin. Environ. Sci. Process Impacts 2013, 15, 1979–2003. [Google Scholar] [CrossRef]
  4. Yang, Y.; Yu, G.; Chen, Y.; Jia, N.; Li, R. Four decades of progress in cylindrospermopsin research: The ins and outs of a potent cyanotoxin. J. Hazard. Mater. 2020, 406, 124653. [Google Scholar] [CrossRef]
  5. Rzymski, P.; Poniedzialek, B. In search of environmental role of cylindrospermopsin: A review on global distribution and ecology of its producers. Water Res. 2014, 66, 320–337. [Google Scholar] [CrossRef] [PubMed]
  6. Scarlett, K.R.; Kim, S.; Lovin, L.M.; Chatterjee, S.; Scott, J.T.; Brooks, B.W. Global scanning of cylindrospermopsin: Critical review and analysis of aquatic occurrence, bioaccumulation, toxicity and health hazards. Sci. Total Environ. 2020, 738, 139807. [Google Scholar] [CrossRef] [PubMed]
  7. Antunes, J.T.; Leao, P.N.; Vasconcelos, V.M. Cylindrospermopsis raciborskii: Review of the distribution, phylogeography, and ecophysiology of a global invasive species. Front. Microbiol. 2015, 6, 473. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  8. Lei, L.; Peng, L.; Huang, X.; Han, B. Occurrence and dominance of Cylindrospermopsis raciborskii and dissolved cylindrospermopsin in urban reservoirs used for drinking water supply, South China. Environ. Monit. Assess. 2014, 186, 3079–3090. [Google Scholar] [CrossRef]
  9. Burford, M.A.; Beardall, J.; Willis, A.; Orr, P.T.; Magalhaes, V.F.; Rangel, L.M.; Azevedo, S.; Neilan, B.A. Understanding the winning strategies used by the bloom-forming cyanobacterium Cylindrospermopsis raciborskii. Harmful Algae 2016, 54, 44–53. [Google Scholar] [CrossRef] [PubMed]
  10. Sinha, R.; Pearson, L.A.; Davis, T.W.; Burford, M.A.; Orr, P.T.; Neilan, B.A. Increased incidence of Cylindrospermopsis raciborskii in temperate zones–Is climate change responsible? Water Res. 2012, 46, 1408–1419. [Google Scholar] [CrossRef]
  11. Moreira, C.; Fathalli, A.; Vasconcelos, V.; Antunes, A. Phylogeny and biogeography of the invasive cyanobacterium Cylindrospermopsis raciborskii. Arch. Microbiol. 2015, 197, 47–52. [Google Scholar] [CrossRef] [PubMed]
  12. Ribeiro, K.F.; Ferrero, A.P.; Duarte, L.; Turchetto-Zolet, A.C.; Crossetti, L.O. Comparative phylogeography of two free-living cosmopolitan cyanobacteria: Insights on biogeographic and latitudinal distribution. J. Biogeogr. 2020, 47, 1106–1118. [Google Scholar] [CrossRef]
  13. Padisák, J. Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium: Worldwide distribution and review of its ecology. Arch. Hydrobiol. Suppl. 1997, 107, 563–593. [Google Scholar]
  14. Vico, P.; Bonilla, S.; Cremella, B.; Aubriot, L.; Iriarte, A.; Piccini, C. Biogeography of the cyanobacterium Raphidiopsis (Cylindrospermopsis) raciborskii: Integrating genomics, phylogenetic and toxicity data. Mol. Phylogenet. Evol. 2020, 148, 106824. [Google Scholar] [CrossRef] [PubMed]
  15. Gugger, M.; Molica, R.; Le Berre, B.; Dufour, P.; Bernard, C.; Humbert, J.-F. Genetic diversity of Cylindrospermopsis strains (Cyanobacteria) isolated from four continents. Appl. Environ. Microbiol. 2005, 71, 1097–1100. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  16. Willis, A.; Woodhouse, J.N.; Ongley, S.E.; Jex, A.R.; Burford, M.A.; Neilan, B.A. Genome variation in nine co-occurring toxic Cylindrospermopsis raciborskii strains. Harmful Algae 2018, 73, 157–166. [Google Scholar] [CrossRef] [PubMed]
  17. Soares, M.C.S.; Lürling, M.; Huszar, V.L.M. Growth and temperature-related phenotypic plasticity in the cyanobacterium Cylindrospermopsis raciborskii. Psychol. Res. 2013, 61, 61–67. [Google Scholar] [CrossRef]
  18. Amaral, V.; Bonilla, S.; Aubriot, L. Growth optimization of the invasive cyanobacterium Cylindrospermopsis raciborskii in response to phosphate fluctuations. Eur. J. Phycol. 2014, 49, 134–141. [Google Scholar] [CrossRef]
  19. Bonilla, S.; Aubriot, L.; Soares, M.C.S.; Gonzalezpiana, M.; Fabre, A.; Huszar, V.L.M.; Lurling, M.; Antoniades, D.; Padisak, J.; Kruk, C. What drives the distribution of the bloom-forming cyanobacteria Planktothrix agardhii and Cylindrospermopsis raciborskii? FEMS Microbiol. Ecol. 2012, 79, 594–607. [Google Scholar] [CrossRef]
  20. Wu, Z.; Yang, S.; Shi, J. Overview of the distribution and adaptation of a bloom-forming cyanobacterium Raphidiopsis raciborskii: Integrating genomics, toxicity, and ecophysiology. J. Oceanol. Limnol. 2022, 40, 1774–1791. [Google Scholar] [CrossRef]
  21. Antosiak, A.; Tokodi, N.; Maziarz, R.; Kokociński, M.; Brzozowska, A.; Strzałka, W.; Banaś, A.K.; Willis, A.; Dziga, D. Different gene expression response of Polish and Australian Raphidiopsis raciborskii strains to the chill/light stress. Appl. Sci. 2020, 10, 5437. [Google Scholar] [CrossRef]
  22. Bonilla, S.; Gonzalez-Piana, M.; Soares, M.C.S.; Huszar, V.L.M.; Becker, V.; Somma, A.; Marinho, M.M.; Kokocinski, M.; Dokulil, M.; Antoniades, D.; et al. The success of the cyanobacterium Cylindrospermopsis raciborskii in freshwaters is enhanced by the combined effects of light intensity and temperature. J. Limnol. 2016, 75, 606–617. [Google Scholar] [CrossRef] [Green Version]
  23. Dokulil, M.T. Vegetative survival of Cylindrospermopsis raciborskii (Cyanobacteria) at low temperature and low light. Hydrobiologia 2016, 764, 241–247. [Google Scholar] [CrossRef]
  24. Tonetta, D.; Hennemann, M.C.; Brentano, D.M.; Petrucio, M.M. Considerations regarding the dominance of Cylindrospermopsis raciborskii under low light availability in a low phosphorus lake. Acta Bot. Bras. 2015, 29, 448–451. [Google Scholar] [CrossRef] [Green Version]
  25. Wojciechowski, J.; Fernandes, L.F.; Buck Fonseca, F.V. Morpho-physiological responses of a subtropical strain of Cylindrospermopsis raciborskii (Cyanobacteria) to different light intensities. Acta Bot. Bras. 2016, 30, 232–238. [Google Scholar] [CrossRef] [Green Version]
  26. Lu, Z.; Ye, J.; Chen, Z.; Xiao, L.; Lei, L.; Han, B.-p.; Paerl, H.W. Cyanophycin accumulated under nitrogen-fluctuating and high-nitrogen conditions facilitates the persistent dominance and blooms of Raphidiopsis raciborskii in tropical waters. Water Res. 2022, 214, 118215. [Google Scholar] [CrossRef]
  27. Willis, A.; Chuang, A.W.; Burford, M.A. Nitrogen fixation by the diazotroph Cylindrospermopsis raciborskii (Cyanophyceae). J. Phycol. 2016, 52, 854–862. [Google Scholar] [CrossRef]
  28. Stucken, K.; John, U.; Cembella, A.; Soto-Liebe, K.; Vasquez, M. Impact of nitrogen sources on gene expression and toxin production in the diazotroph Cylindrospermopsis raciborskii CS-505 and non-diazotroph Raphidiopsis brookii D9. Toxins 2014, 6, 1896–1915. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  29. Moisander, P.H.; Cheshire, L.A.; Braddy, J.; Calandrino, E.S.; Hoffman, M.; Piehler, M.F.; Paerl, H.W. Facultative diazotrophy increases Cylindrospermopsis raciborskii competitiveness under fluctuating nitrogen availability. FEMS Microbiol. Ecol. 2012, 79, 800–811. [Google Scholar] [CrossRef] [Green Version]
  30. Wu, Z.; Shi, J.; Li, R. Comparative studies on photosynthesis and phosphate metabolism of Cylindrospermopsis raciborskii with Microcystis aeruginosa and Aphanizomenon flos-aquae. Harmful Algae 2009, 8, 910–915. [Google Scholar] [CrossRef]
  31. Wu, Z.; Zeng, B.; Li, R.; Song, L. Physiological regulation of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) in response to inorganic phosphorus limitation. Harmful Algae 2012, 15, 53–58. [Google Scholar] [CrossRef]
  32. Shi, J.-q.; Ou-yang, T.; Yang, S.-q.; Zhao, L.; Ji, L.-l.; Wu, Z.-x. Transcriptomic responses to phosphorus in an invasive cyanobacterium, Raphidiopsis raciborskii: Implications for nutrient management. Harmful Algae 2022, 111, 102150. [Google Scholar] [CrossRef] [PubMed]
  33. Chislock, M.F.; Sharp, K.L.; Wilson, A.E. Cylindrospermopsis raciborskii dominates under very low and high nitrogen-to-phosphorus ratios. Water Res. 2014, 49, 207–214. [Google Scholar] [CrossRef] [PubMed]
  34. Bai, F.; Shi, J.; Yang, S.; Yang, Y.; Wu, Z. Interspecific competition between Cylindrospermopsis raciborskii and Microcystis aeruginosa on different phosphorus substrates. Environ. Sci. Pollut. Res. 2020, 27, 42264–42275. [Google Scholar] [CrossRef]
  35. Jia, N.; Yang, Y.; Yu, G.; Wang, Y.; Qiu, P.; Li, H.; Li, R. Interspecific competition reveals Raphidiopsis raciborskii as a more successful invader than Microcystis aeruginosa. Harmful Algae 2020, 97, 101858. [Google Scholar] [CrossRef]
  36. Rzymski, P.; Poniedzialek, B.; Kokocinski, M.; Jurczak, T.; Lipski, D.; Wiktorowicz, K. Interspecific allelopathy in cyanobacteria: Cylindrospermopsin and Cylindrospermopsis raciborskii effect on the growth and metabolism of Microcystis aeruginosa. Harmful Algae 2014, 35, 1–8. [Google Scholar] [CrossRef]
  37. Campos, A.; Araujo, P.; Pinheiro, C.; Azevedo, J.; Osorio, H.; Vasconcelos, V. Effects on growth, antioxidant enzyme activity and levels of extracellular proteins in the green alga Chlorella vulgaris exposed to crude cyanobacterial extracts and pure microcystin and cylindrospermopsin. Ecotoxicol. Environ. Saf. 2013, 94, 45–53. [Google Scholar] [CrossRef]
  38. Bbéres, V.; Vasas, G.; Dobronoki, D.; Gonda, S.; Nagy, S.A.; Bácsi, I. Effects of cylindrospermopsin producing cyanobacterium and its crude extracts on a benthic green alga-competition or allelopathy? Mar. Drugs 2015, 13, 6703–6722. [Google Scholar] [CrossRef] [Green Version]
  39. Bar-Yosef, Y.; Sukenik, A.; Hadas, O.; Viner-Mozzini, Y.; Kaplan, A. Enslavement in the water body by toxic Aphanizomenon ovalisporum, inducing alkaline phosphatase in phytoplanktons. Curr. Biol. 2010, 20, 1557–1561. [Google Scholar] [CrossRef] [Green Version]
  40. Burford, M.A.; Willis, A.; Chuang, A.; Man, X.; Orr, P.T. Recent insights into physiological responses to nutrients by the cylindrospermopsin producing cyanobacterium, Cylindrospermopsis raciborskii. Chin. J. Oceanol. Limnol. 2018, 36, 1032–1039. [Google Scholar] [CrossRef] [Green Version]
  41. Xiao, M.; Hamilton, D.P.; Chuang, A.; Burford, M.A. Intra-population strain variation in phosphorus storage strategies of the freshwater cyanobacterium Raphidiopsis raciborskii. FEMS Microbiol. Ecol. 2020, 96, fiaa092. [Google Scholar] [CrossRef] [PubMed]
  42. Sinha, R.; Pearson, L.A.; Davis, T.W.; Muenchhoff, J.; Pratama, R.; Jex, A.; Burford, M.A.; Neilan, B.A. Comparative genomics of Cylindrospermopsis raciborskii strains with differential toxicities. BMC Genom. 2014, 15, 83. [Google Scholar] [CrossRef] [Green Version]
  43. Guedes, L.A.; Pacheco, A.B.F.; Vilar, M.C.P.; Mello, M.M.; Marinho, M.M.; Lurling, M.; Azevedo, S.M.F.O. Intraspecific variability in response to phosphorus depleted conditions in the cyanobacteria Microcystis aeruginosa and Raphidiopsis raciborskii. Harmful Algae 2019, 86, 96–105. [Google Scholar] [CrossRef]
  44. Lei, L.; Dai, J.; Lin, Q. Competitive dominance of Microcystis aeruginosa against Raphidiopsis raciborskii is strain- and temperature-dependent. Knowl. Manag. Aquat. Ecosyst. 2020, 421, 36. [Google Scholar] [CrossRef]
  45. Marinho, M.M.; Souza, M.B.G.; Lurling, M. Light and phosphate competition between Cylindrospermopsis raciborskii and Microcystis aeruginosa is strain dependent. Microb. Ecol. 2013, 66, 479–488. [Google Scholar] [CrossRef] [PubMed]
  46. Ma, Z.; Zhang, X.; Li, R.; Wang, M.; Qin, W.; Zhang, H.; Li, G.; Yu, H.; Dai, C.; Zhao, M. Competitiveness of alga Microcystis aeruginosa co-cultivated with cyanobacterium Raphidiopsis raciborskii confirms its dominating position. J. Oceanol. Limnol. 2022, 40, 1804–1818. [Google Scholar] [CrossRef]
  47. Jia, N.; Wang, Y.; Guan, Y.; Chen, Y.; Li, R.; Yu, G. Occurrence of Raphidiopsis raciborskii blooms in cool waters: Synergistic effects of nitrogen availability and ecotypes with adaptation to low temperature. Environ. Pollut. 2021, 270, 116070. [Google Scholar] [CrossRef]
  48. Jiang, Y.; Xiao, P.; Yu, G.; Shao, J.; Liu, D.; Azevedo, S.M.F.O.; Li, R. Sporadic distribution and distinctive variations of cylindrospermopsin genes in cyanobacterial strains and environmental samples from Chinese freshwater bodies. Appl. Environ. Microbiol. 2014, 80, 5219–5230. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  49. Wu, Z.; Shi, J.; Xiao, P.; Liu, Y.; Li, R. Phylogenetic analysis of two cyanobacterial genera Cylindrospermopsis and Raphidiopsis based on multi-gene sequences. Harmful Algae 2011, 10, 419–425. [Google Scholar] [CrossRef]
  50. Xie, J.; Yu, G.; Xu, X.; Li, S.; Li, R. The morphological and molecular detection for the presence of toxic Cylindrospermopsis (Nostocales, Cyanobacteria) in Beijing city, China. J. Oceanol. Limnol. 2018, 36, 263–272. [Google Scholar] [CrossRef]
  51. Huo, D.; Gan, N.; Geng, R.; Cao, Q.; Song, L.; Yu, G.; Li, R. Cyanobacterial blooms in China: Diversity, distribution, and cyanotoxins. Harmful Algae 2021, 109, 102106. [Google Scholar] [CrossRef] [PubMed]
  52. Yamamoto, Y.; Shiah, F.-K. Factors related to the dominance of Cylindrospermopsis raciborskii (cyanobacteria) in a shallow pond in northern Taiwan. J. Phycol. 2012, 48, 984–991. [Google Scholar] [CrossRef]
  53. Zha, G. Investigation on the ecological factor in Cylindrospermopsis raciborskii bloom in low salty prawn ponds. Ecol. Sci. 2009, 28, 293–298. (In Chinese) [Google Scholar] [CrossRef]
  54. Schmidt, B.V.; Wang, Z.; Ren, P.; Guo, C.; Qin, J.; Cheng, F.; Xie, S. A review of potential factors promoting fish movement in inter-basin water transfers, with emergent patterns from a trait-based risk analysis for a large-scale project in china. Ecol. Freshw. Fish 2020, 29, 790–807. [Google Scholar] [CrossRef]
  55. Atkinson, K.M. Experiments in dispersal of phytoplankton by ducks. Eur. J. Phycol. 1980, 15, 49–58. [Google Scholar] [CrossRef]
  56. Mihali, T.K.; Kellmann, R.; Muenchhoff, J.; Barrow, K.D.; Neilan, B.A. Characterization of the gene cluster responsible for cylindrospermopsin biosynthesis. Appl. Environ. Microbiol. 2008, 74, 716–722. [Google Scholar] [CrossRef] [Green Version]
  57. Fan, D.; Lei, S.; Liang, H.; Yao, Q.; Kou, Y.; Cheng, S.; Yang, Y.; Qiu, Y.; Zhang, Z. More opportunities more species: Pleistocene differentiation and northward expansion of an evergreen broad-leaved tree species Machilus thunbergii (Lauraceae) in Southeast China. BMC Plant Biol. 2022, 22, 35. [Google Scholar] [CrossRef] [PubMed]
  58. Jiang, Y.; Chen, Y.; Yang, S.; Li, R. Phylogenetic relationships and genetic divergence of paralytic shellfish toxin- and cylindrospermopsin- producing Cylindrospermopsis and Raphidiopsis. Harmful Algae 2020, 93, 101792. [Google Scholar] [CrossRef]
  59. Chen, Y. Distribution, Molecular Characteristics and Monitoring of Neurotoxin-Producing Cyanobacteria in China. Ph.D. Thesis, University of Chinese Academy of Sciences, Wuhan, China, 2018. [Google Scholar]
  60. Chonudomkul, D.; Yongmanitchai, W.; Theeragool, G.; Kawachi, M.; Kasai, F.; Kaya, K.; Watanabe, M.M. Morphology, genetic diversity, temperature tolerance and toxicity of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) strains from Thailand and Japan. FEMS Microbiol. Ecol. 2004, 48, 345–355. [Google Scholar] [CrossRef]
  61. Piccini, C.; Aubriot, L.; Fabre, A.; Amaral, V.; González-Piana, M.; Giani, A.; Figueredo, C.C.; Vidal, L.; Kruk, C.; Bonilla, S. Genetic and eco-physiological differences of South American Cylindrospermopsis raciborskii isolates support the hypothesis of multiple ecotypes. Harmful Algae 2011, 10, 644–653. [Google Scholar] [CrossRef]
  62. Briand, J.-F.; Leboulanger, C.; Humbert, J.-F.; Bernard, C.; Dufour, P. Cylindrospermopsis raciborskii (cyanobacteria) invasion at mid-latitudes: Selection, wide physiological tolerance, or global warming? J. Phycol. 2004, 40, 231–238. [Google Scholar] [CrossRef]
  63. Pierangelini, M.; Stojkovic, S.; Orr, P.T.; Beardall, J. Photosynthetic characteristics of two Cylindrospermopsis raciborskii strains differing in their toxicity. J. Phycol. 2014, 50, 292–302. [Google Scholar] [CrossRef] [PubMed]
  64. Neves de Lima, D.V.; Furlanetto Pacheco, A.B.; Goulart, C.L.; de Oliveira e Azevedo, S.M.F. Physiological responses of Raphidiopsis raciborskii (Cyanobacteria) strains to water conductivity: Effect of sodium and magnesium ions. Hydrobiologia 2020, 847, 2449–2464. [Google Scholar] [CrossRef]
  65. Willis, A.; Chuang, A.W.; Woodhouse, J.N.; Neilan, B.A.; Burford, M.A. Intraspecific variation in growth, morphology and toxin quotas for the cyanobacterium, Cylindrospermopsis raciborskii. Toxicon 2016, 119, 307–310. [Google Scholar] [CrossRef]
  66. Saker, M.L.; Neilan, B.A. Varied diazotrophies, morphologies, and toxicities of genetically similar isolates of Cylindrospermopsis raciborskii (Nostocales, Cyanophyceae) from Northern Australia. Appl. Environ. Microbiol. 2001, 67, 1839–1845. [Google Scholar] [CrossRef] [Green Version]
  67. Li, X.; Li, S.; Kong, R.; Li, R. Molecular separation of two long taxonomically debated cyanobacterial genera Cylindrospermopsis and Raphidiopsis (Nostocales) based on the ITS-L phylogeny. Harmful Algae 2016, 57, 88–97. [Google Scholar] [CrossRef] [Green Version]
  68. Abreu, V.A.C.; Popin, R.V.; Alvarenga, D.O.; Schaker, P.D.C.; Hoff-Risseti, C.; Varani, A.M.; Fiore, M.F. Genomic and genotypic characterization of Cylindrospermopsis raciborskii: Toward an intraspecific phylogenetic evaluation by comparative genomics. Front. Microbiol. 2018, 9, 306. [Google Scholar] [CrossRef]
  69. Lei, L.; Lei, M.; Cheng, N.; Chen, Z.; Xiao, L.; Han, B.; Lin, Q. Nutrient regulation of relative dominance of cylindrospermopsin-producing and non-cylindrospermopsin-producing Raphidiopsis raciborskii. Front. Microbiol. 2021, 12, 793544. [Google Scholar] [CrossRef]
  70. Burford, M.A.; Davis, T.W.; Orr, P.T.; Sinha, R.; Willis, A.; Neilan, B.A. Nutrient-related changes in the toxicity of field blooms of the cyanobacterium, Cylindrospermopsis raciborskii. FEMS Microbiol. Ecol. 2014, 89, 135–148. [Google Scholar] [CrossRef] [Green Version]
  71. D’Agostino, P.M.; Yeung, A.C.Y.; Poljak, A.; David Waite, T.; Neilan, B.A. Comparative proteomics of the toxigenic diazotroph Raphidiopsis raciborskii (cyanobacteria) in response to iron. Environ. Microbiol. 2021, 23, 405–414. [Google Scholar] [CrossRef]
  72. Willis, A.; Adams, M.P.; Chuang, A.W.; Orr, P.T.; O’Brien, K.R.; Burford, M.A. Constitutive toxin production under various nitrogen and phosphorus regimes of three ecotypes of Cylindrospermopsis raciborskii ((Woloszyriska) Seenayya et Subba Raju). Harmful Algae 2015, 47, 27–34. [Google Scholar] [CrossRef]
  73. Mazmouz, R.; Chapuis-Hugon, F.; Pichon, V.; Mejean, A.; Ploux, O. The last step of the biosynthesis of the cyanotoxins cylindrospermopsin and 7-epi-cylindrospermopsin is catalysed by CyrI, a 2-Oxoglutarate-dependent iron oxygenase. ChemBioChem 2011, 12, 858–862. [Google Scholar] [CrossRef] [PubMed]
  74. Mazmouz, R.; Essadik, I.; Hamdane, D.; Méjean, A.; Ploux, O. Characterization of CyrI, the hydroxylase involved in the last step of cylindrospermopsin biosynthesis: Binding studies, site-directed mutagenesis and stereoselectivity. Arch. Biochem. Biophys. 2018, 647, 1–9. [Google Scholar] [CrossRef] [PubMed]
  75. Méjean, A.; Ploux, O. Biosynthesis of cylindrospermopsin in cyanobacteria: Characterization of CyrJ the sulfotransferase. J. Nat. Prod. 2021, 84, 408–416. [Google Scholar] [CrossRef] [PubMed]
  76. Jiang, Y.; Xiao, P.; Yu, G.; Sano, T.; Pan, Q.; Li, R. Molecular basis and phylogenetic implications of deoxycylindrospermopsin biosynthesis in the cyanobacterium Raphidiopsis curvata. Appl. Environ. Microbiol. 2012, 78, 2256–2263. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  77. Xiao, M.; Li, M.; Reynolds, C.S. Colony formation in the cyanobacterium Microcystis. Biol. Rev. 2018, 93, 1399–1420. [Google Scholar] [CrossRef] [Green Version]
  78. Xiao, M.; Adams, M.P.; Willis, A.; Burford, M.A.; O’Brien, K.R. Variation within and between cyanobacterial species and strains affects competition: Implications for phytoplankton modelling. Harmful Algae 2017, 69, 38–47. [Google Scholar] [CrossRef]
  79. da Silva Brito, M.T.; Duarte-Neto, P.J.; Reis Molica, R.J. Cylindrospermopsis raciborskii and Microcystis aeruginosa competing under different conditions of pH and inorganic carbon. Hydrobiologia 2018, 815, 253–266. [Google Scholar] [CrossRef]
  80. Hendry, A.P.; Kinnison, M.T. An introduction to microevolution: Rate, pattern, process. Genetica 2001, 112, 1–8. [Google Scholar] [CrossRef]
  81. Sidelev, S.; Koksharova, O.; Babanazarova, O.; Fastner, J.; Chernova, E.; Gusev, E. Phylogeographic, toxicological and ecological evidence for the global distribution of Raphidiopsis raciborskii and its northernmost presence in Lake Nero, Central Western Russia. Harmful Algae 2020, 98, 101889. [Google Scholar] [CrossRef]
  82. Li, S.-p.; Tan, J.; Yang, X.; Ma, C.; Jiang, L. Niche and fitness differences determine invasion success and impact in laboratory bacterial communities. ISME J. 2019, 13, 402–412. [Google Scholar] [CrossRef] [PubMed]
  83. Yang, Y.; Jiang, Y.; Li, X.; Li, H.; Chen, Y.; Xie, J.; Cai, F.; Li, R. Variations of growth and toxin yield in Cylindrospermopsis raciborskii under different phosphorus concentrations. Toxins 2017, 9, 13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  84. Aguilera, A.; Aubriot, L.; Echenique, R.O.; Donadelli, J.L.; Salerno, G.L. Raphidiopsis mediterranea (Nostocales) exhibits a flexible growth strategy under light and nutrient fluctuations in contrast to Planktothrix agardhii (Oscillatoriales). Hydrobiologia 2019, 839, 145–157. [Google Scholar] [CrossRef]
  85. Lu, Z.; Lei, L.; Lu, Y.; Peng, L.; Han, B. Phosphorus deficiency stimulates dominance of Cylindrospermopsis through facilitating cylindrospermopsin-induced alkaline phosphatase secretion: Integrating field and laboratory-based evidences. Environ. Pollut. 2021, 290, 117946. [Google Scholar] [CrossRef]
  86. Bolius, S.; Wiedner, C.; Weithoff, G. Low invasion success of an invasive cyanobacterium in a chlorophyte dominated lake. Sci. Rep. 2019, 9, 8297. [Google Scholar] [CrossRef] [Green Version]
  87. Tilahun, S.; Kifle, D. The influence of El Niño-induced drought on cyanobacterial community structure in a shallow tropical reservoir (Koka Reservoir, Ethiopia). Aquat. Ecol. 2019, 53, 61–77. [Google Scholar] [CrossRef]
  88. Weithoff, G.; Taube, A.; Bolius, S. The invasion success of the cyanobacterium Cylindrospermopsis raciborskii in experimental mesocosms: Genetic identity, grazing loss, competition and biotic resistance. Aquat. Invasions 2017, 12, 333–341. [Google Scholar] [CrossRef]
  89. Ferrão-Filho, A.S.; Pereira, U.J.; Vilar, M.C.P.; de Magalhães, L.; Marinho, M.M. Can small-bodied Daphnia control Raphidiopsis raciborskii in eutrophic tropical lakes? A mesocosm experiment. Environ. Sci. Pollut. Res. 2020, 27, 35459–35473. [Google Scholar] [CrossRef]
  90. Hong, Y.; Burford, M.A.; Ralph, P.J.; Udy, J.W.; Doblin, M.A. The cyanobacterium Cylindrospermopsis raciborskii is facilitated by copepod selective grazing. Harmful Algae 2013, 29, 14–21. [Google Scholar] [CrossRef]
  91. Ferrao-Filho, A.D.S.; Dias, T.M.; Pereira, U.J.; dos Santos, J.A.A.; Kozlowsky-Suzuki, B. Nutritional and toxicity constraints of phytoplankton from a Brazilian reservoir to the fitness of cladoceran species. Environ. Sci. Pollut. Res. 2019, 26, 12881–12893. [Google Scholar] [CrossRef]
  92. Li, X.; Huo, S.; Zhang, J.; Xiao, Z.; Xi, B.; Li, R. Factors related to aggravated Cylindrospermopsis (cyanobacteria) bloom following sediment dredging in an eutrophic shallow lake. Environ. Sci. Ecotechnol. 2020, 2, 100014. [Google Scholar] [CrossRef] [PubMed]
  93. Lakeman, M.B.; von Dassow, P.; Cattolico, R.A. The strain concept in phytoplankton ecology. Harmful Algae 2009, 8, 746–758. [Google Scholar] [CrossRef]
  94. Wang, Y. Variation of cyanobacteria community and in the main regulating reservoirs in Shandong province and the growth characteristics of Cylindrospermopsis. Master’s Thesis, Shandong University, Jinan, China, 2018. (In Chinese). [Google Scholar]
  95. Zheng, H. Risk assessment of cyanobacterial blooms in drinking water reservoirs of Fujian province. Hua Xue Gong Cheng Yu Zhuang Bei 2012, 201–203. (In Chinese) [Google Scholar] [CrossRef]
  96. Gao, X.; Wang, W.; Ndayishimiye, J.C.; Govaert, L.; Chen, H.; Jeppesen, E.; Xue, Y.; Yu, X.; Yang, J. Invasive and toxic cyanobacteria regulate allochthonous resource use and community niche width of reservoir zooplankton. Freshw. Biol. 2022, 67, 1344–1356. [Google Scholar] [CrossRef]
  97. Zheng, H. Characteristics of phytoplankton community and nutrient conditions in Dongzhen reservoir. Hua Xue Gong Cheng Yu Zhuang Bei 2012, 193–195+200. (In Chinese) [Google Scholar] [CrossRef]
  98. Jiang, Y.; Xiao, P.; Liu, Y.; Wang, J.; Li, R. Targeted deep sequencing reveals high diversity and variable dominance of bloom-forming cyanobacteria in eutrophic lakes. Harmful Algae 2017, 64, 42–50. [Google Scholar] [CrossRef]
  99. Wang, Z.F.; Zhang, W.; Yang, L.; Xu, Y.P.; Zhao, F.B.; Wang, L.Q. Characteristics of phytoplankton community and its relationship with environmental factors in different regions of Yilong Lake, Yunnan Province, China. Huan Jing Ke Xue 2019, 40, 2249–2257. (In Chinese) [Google Scholar] [CrossRef]
  100. Wang, X.; Li, Q.; Chen, W.; Han, M.; Han, L.; Brancelj, A. Composition and indication of plankton fatty acids under the influence of environmental factors in the Hongfeng Reservoir, Southwest China. Aquat. Ecol. 2022, 56, 653–666. [Google Scholar] [CrossRef]
  101. Ouyang, T.; Yang, S.; Zhao, L.; Ji, L.; Shi, J.; Wu, Z. Temporal heterogeneity of bacterial communities and their responses to Raphidiopsis raciborskii blooms. Microbiol. Res. 2022, 262, 127098. [Google Scholar] [CrossRef]
  102. Wu, D.; Xu, Z.; Wang, Y.; Gao, Y. Seasonal variation of phytoplankton community structure in Hengshan reservoir. Shui Sheng Tai Xue Za Zhi 2012, 33, 54–57. (In Chinese) [Google Scholar] [CrossRef]
  103. Zou, H.; Hu, R.; Han, B. Structure and dynamics of phytoplankton community in Hedi Reservoir, South China. J. Trop. Subtrop. Botany 2010, 18, 196–202. (In Chinese) [Google Scholar] [CrossRef]
  104. Lei, M.; Peng, L.; Han, B.; Lei, L. Distribution and affecting factors of Cylindrospermopsis raciborskii in Guangdong reservoirs. Huan Jing Ke Xue 2018, 39, 5523–5531. (In Chinese) [Google Scholar] [CrossRef] [PubMed]
  105. Zhao, L.; Lei, L.; Peng, L.; Han, B. Seasonal dynamic and driving factors of Cylindrospermopsis raciborskii in Zhenhai Reservoir, Guangdong Province. Hu Po Ke Xue 2017, 29, 193–199. (In Chinese) [Google Scholar] [CrossRef] [Green Version]
  106. Xue, X.; Fang, G.; Zou, C.; Zhu, D.; Xiao, L.; Peng, L. Diel vertical distribution patterns of Raphidiopsis raciborskii in Dashahe Reservoir. Sheng Tai Xue Za Zhi 2020, 39, 2348–2355. (In Chinese) [Google Scholar] [CrossRef]
  107. Lu, Y.; Lei, M.; Ye, J.; Lei, L.; Han, B. Intraspecific variation of morphological traits and toxin-producing capacity and phylogenetic analysis for Cylindrospermopsis raciborskii from Qiandenghu Lake, Guangdong Province. Hu Po Ke Xue 2020, 32, 144–153. (In Chinese) [Google Scholar] [CrossRef]
  108. Tang, H.; Liu, P.; Wu, J.; Liao, H.; He, A. Phytoplankton functional groups and their response to physiochemical factors in Hongchaojiang Reservoir in Guangxi Province. Shui Sheng Tai Xue Za Zhi 2022, 1–13. (In Chinese) [Google Scholar] [CrossRef]
Ijerph 20 01984 g001 550
Figure 1. Cell differentiation of R. raciborskii filament (A), aerial view of the R. raciborskii bloom (B), and chemical structure of cylindrospermopsins (C). Inset in (B) is a microscopic graph of R. raciborskii bloom. Scale bars in (A,B), 10 µm.
Figure 1. Cell differentiation of R. raciborskii filament (A), aerial view of the R. raciborskii bloom (B), and chemical structure of cylindrospermopsins (C). Inset in (B) is a microscopic graph of R. raciborskii bloom. Scale bars in (A,B), 10 µm.
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Figure 2. Distribution of R. raciborskii in major river basins of China. A, Haihe River basin; B, Huanghe River basin; C, Huaihe River basin; D, Yangtze River basin; E, Zhujiang River basin; F, basins of southeastern rivers. Blue-green color, areas with presence of R. raciborskii.
Figure 2. Distribution of R. raciborskii in major river basins of China. A, Haihe River basin; B, Huanghe River basin; C, Huaihe River basin; D, Yangtze River basin; E, Zhujiang River basin; F, basins of southeastern rivers. Blue-green color, areas with presence of R. raciborskii.
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Figure 3. Probable dispersion routes for R. raciborskii.
Figure 3. Probable dispersion routes for R. raciborskii.
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Table
Table 1. Types of cyrI and cyrJ sequences from Chinese water bodies.
Table 1. Types of cyrI and cyrJ sequences from Chinese water bodies.
Water BodyLatitude (N), Longitude (E)cyrIcyrJ
Liangzi lake, Ezhou, Hubei114°31′ E, 30°15′ NItype2Not detected
Qiaodun lake, Daye, Hubei114°43′ E, 30°14′ NItype4afJtype2a
Chidong lake, Qichun, Hubei115°25′ E, 30°06′ NItype4af, Itype4arJtype2a
Xianghu lake, Hangzhou, Zhejiang120°12′ E, 30°7′ NItype1Jtype2a
Qiandao lake, Hangzhou, Zhejiang118°57′ E, 29°33′ NItype2Jtype2a, Jtype2b
Dongzhen reservoir, Putian, Fujian118°57′ E, 25°29′ NItype3Jtype1
Shiyan reservoir, Shenzhen113°54′ E, 22°42′ NItype1Jtype1, Jtype2b
Tiegang reservoir, Shenzhen113°53′ E, 22°37′ NItype1, Itype2, Itype3Jtype1, Jtype2a, Jtype3
Table
Table 2. Results of competition experiments using R. raciborskii and M. aeruginosa.
Table 2. Results of competition experiments using R. raciborskii and M. aeruginosa.
Strain Pair and Culture ConditionDominant StrainReference
R. raciborskii FACHB 1096 vs. M. aeruginosa strain 205
P substratesK2HPO4, β-glycerol phosphate, (2-aminoethyl)-phosphinic acid, P-freeR. raciborskii FACHB 1096[34]
GlyphosateM. aeruginosa strain 205
R. raciborskii CS vs. M. aeruginosa LEA
P and lightP-limitationR. raciborskii CS[45]
Light-limitationR. raciborskii CS
R. raciborskii CP vs. M. aeruginosa MIRF
P and lightP-limitationM. aeruginosa MIRF[45]
Light-limitationM. aeruginosa MIRF
R. raciborskii N8 vs. M. aeruginosa FACHB905
Temperature16 °C, 24 °C, 32 °CM. aeruginosa FACHB905[44]
R. raciborskii N8 vs. M. aeruginosa (FACHB469 and 915) with a biovolume ratio of 30:1
Temperature16 °C, 24 °C, 32 °CR. raciborskii N8 maintained initial advantages at 16 °C and 32 °C[44]
M. aeruginosa strains at 24 °C
R. raciborskii ITEP-A1 vs. M. aeruginosa NPLJ-4
pH and inorganic carbonAerationR. raciborskii ITEP-A1[79]
BicarbonateM. aeruginosa NPLJ-4
R. raciborskii NW-R vs. M. aeruginosa NW-M
Growth capabilityMultiple inoculation ratiosR. raciborskii NW-R[35]
Four M. aeruginosa vs. eight R. raciborskii strains
Growth capabilitySimulated using a deterministic modelNo absolute winner[78]
Table
Table 3. Adaptation of R. raciborskii to different ecological scenarios.
Table 3. Adaptation of R. raciborskii to different ecological scenarios.
ScenariosLevelResponseConsequence
Climate warmingHigher temperatureGrowth promotionBiomass increase and dispersion to new habitats
P fluctuationLow concentrationALP or CYN secretionBecome dominant
High concentrationHigh P absorptionBiomass increase
N fluctuationLow concentrationN fixationBecome dominant
High concentrationHeterocyst inhibition and N absorptionBiomass increase
Grazing pressureGrazer feeding on R. raciborskiiGrowth inhibitionBiomass decrease
Grazer feeding on non-R. raciborskii phytoplanktonGrowth promotionBecome dominant
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Zheng, L.; Liu, Y.; Li, R.; Yang, Y.; Jiang, Y. Recent Advances in the Ecology of Bloom-Forming Raphidiopsis (Cylindrospermopsis) raciborskii: Expansion in China, Intraspecific Heterogeneity and Critical Factors for Invasion. Int. J. Environ. Res. Public Health 2023, 20, 1984. https://0-doi-org.brum.beds.ac.uk/10.3390/ijerph20031984

AMA Style

Zheng L, Liu Y, Li R, Yang Y, Jiang Y. Recent Advances in the Ecology of Bloom-Forming Raphidiopsis (Cylindrospermopsis) raciborskii: Expansion in China, Intraspecific Heterogeneity and Critical Factors for Invasion. International Journal of Environmental Research and Public Health. 2023; 20(3):1984. https://0-doi-org.brum.beds.ac.uk/10.3390/ijerph20031984

Chicago/Turabian Style

Zheng, Ling, Yang Liu, Renhui Li, Yiming Yang, and Yongguang Jiang. 2023. "Recent Advances in the Ecology of Bloom-Forming Raphidiopsis (Cylindrospermopsis) raciborskii: Expansion in China, Intraspecific Heterogeneity and Critical Factors for Invasion" International Journal of Environmental Research and Public Health 20, no. 3: 1984. https://0-doi-org.brum.beds.ac.uk/10.3390/ijerph20031984

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