Intraspecific Heterogeneity: Comparison
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Intraspecific heterogeneity describes the phenotypic and genetic diversity within the population of a species. Intraspecific heterogeneity is derived from microevolution and is a strong driving force for the expansion of invasive species such as the bloom-forming cyanobacterium Raphidiopsis raciborskii.

  • cylindrospermopsin
  • microbial invasion
  • microevolution
  • nutrient fluctuations

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].
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.

2. 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][13][14][15]. 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 [16][17]. 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][18][19] and conductivity [20], as well as its strategies for the utilization of N [21][22] and P [23]. In addition, varied growth rates, morphologies, and toxicities have been observed in genetically similar isolates of R. raciborskii [24][25].
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 [26][27]. The strains were classified into nontoxic, CYN-producing, and PSP-producing clusters based on the phylogenetic analysis of rpoC1 and ITS-L [26]. This result is supported by the genomic variations between R. raciborskii strains [28][29][30]. 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 [31]. However, genomic variations were also found in genes associated with stress and adaptation, which are probably related to the physiological role of CYN [29]. 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 [32]. In comparison to nontoxic R. raciborskii, toxic strains have a more efficient response to inorganic phosphorus and could become dominant in the community [33]. A recent study also found that toxic strains were more competitive under Fe-starved conditions [34].
Previous investigations have revealed that the cell quotas of CYN varied significantly between R. raciborskii strains [24][25][35]. 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 [31][36][37][38]. These two enzymes catalyze tailoring reactions in the last two steps of CYN biosynthesis [39]. An inactivated mutation of cyrI inhibits the synthesis of CYN, leading to an accumulation in the intermediate product 7-deoxy-CYN [40]. Therefore, variations in cyr genes may change the activity of the enzymes encoded by them and further affect CYN synthesis efficiency.

3. Competition between R. raciborskii and M. aeruginosa

M. aeruginosa is the dominant species in most eutrophic water bodies, both in China and worldwide [41][42]. 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 21). 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 [43]. R. raciborskii, with N-fixation capability, was a more successful invader than M. aeruginosa when N was depleted in batch culture [44]. Likewise, the model prediction of species competition outcomes is strongly affected by the growth variability of strains [45]. These findings demonstrate the intraspecific heterogeneity for R. raciborskii and M. aeruginosa [46].
Table 21.
Results of competition experiments using
R. raciborskii
and
M. aeruginosa
.
Strain Pair and Culture Condition Dominant Strain Reference
R. raciborskii FACHB 1096 vs. M. aeruginosa strain 205
P substrates K2HPO4, β-glycerol phosphate, (2-aminoethyl)-phosphinic acid, P-free R. raciborskii FACHB 1096 [47]
Glyphosate M. aeruginosa strain 205
R. raciborskii CS vs. M. aeruginosa LEA
P and light P-limitation R. raciborskii CS [43]
Light-limitation R. raciborskii CS
R. raciborskii CP vs. M. aeruginosa MIRF
P and light P-limitation M. aeruginosa MIRF [43]
Light-limitation M. aeruginosa MIRF
R. raciborskii N8 vs. M. aeruginosa FACHB905
Temperature 16 °C, 24 °C, 32 °C M. aeruginosa FACHB905 [46]
R. raciborskii N8 vs. M. aeruginosa (FACHB469 and 915) with a biovolume ratio of 30:1
Temperature 16 °C, 24 °C, 32 °C R. raciborskii N8 maintained initial advantages at 16 °C and 32 °C [46]
M. aeruginosa strains at 24 °C
R. raciborskii ITEP-A1 vs. M. aeruginosa NPLJ-4
pH and inorganic carbon Aeration R. raciborskii ITEP-A1 [48]
Bicarbonate M. aeruginosa NPLJ-4
R. raciborskii NW-R vs. M. aeruginosa NW-M
Growth capability Multiple inoculation ratios R. raciborskii NW-R [44]
Four M. aeruginosa vs. eight R. raciborskii strains
Growth capability Simulated using a deterministic model No absolute winner [45]

4. 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 [14][15][35]. 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 [24][28]. Heterogeneity between coexisting strains is better defined as microevolution, the concept of which refers to minor variations within species [49]. 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.

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