Phenotypically Different Microalgal Morphospecies with Identical Ribosomal DNA: A Case of Rapid Adaptive Evolution?

Abstract

The agents driving the divergence and speciation of free-living microbial populations are still largely unknown. We investigated the dinoflagellate morphospecies Scrippsiella hangoei and Peridinium aciculiferum, which abound in the Baltic Sea and in northern temperate lakes, respectively. Electron microscopy analyses showed significant interspecific differences in the external cellular morphology, but a similar plate pattern in the characteristic dinoflagellate armor. Experimentally, S. hangoei grew in a wide range of salinities (0-30), whereas P. aciculiferum only grew in low salinities (0-3). Despite these phenotypic differences and the habitat segregation, molecular analyses showed identical ribosomal DNA sequences (ITS1, ITS2, 5.8S, SSU, and partial LSU) for both morphospecies. Yet, a strong interspecific genetic isolation was indicated by amplified fragment length polymorphism (F (ST) = 0.76) and cytochrome b (cob) sequence divergence ( approximately 1.90%). Phylogenetic reconstructions based on ribosomal (SSU, LSU) and mitochondrial (cob) DNA indicated a recent marine ancestor for P. aciculiferum. In conclusion, we suggest that the lacustrine P. aciculiferum and the marine-brackish S. hangoei diverged very recently, after a marine-freshwater transition that exposed the ancestral populations to different selective pressures. This hypothetical scenario agrees with mounting data indicating a significant role of natural selection in the divergence of free-living microbes, despite their virtually unrestricted dispersal capabilities. Finally, our results indicate that identical ITS rDNA sequences do not necessarily imply the same microbial species, as commonly assumed.

Recent radiation in a marine and freshwater dinoflagellate species flock

“…Phylogenetic trees based on the ITS2 and COB fragments confirmed the closeness of the studied dinoflagellates with Pfiesteria-like species (data not shown) in agreement with rDNA tree and an earlier phylogeny by Logares et al (2007a). Figure 7 Phylogenetic analysis based on partial SSU rRNA gene and partial LSU rRNA gene.…”

“…In the current case, all four morphospecies occur in freshwater lakes, except S. hangoei, which has a wide salinity tolerance and is also found in the Baltic Sea and polar oceans. Previously, Logares et al (2007aLogares et al ( , 2008) described a close relationship between the marine S. hangoei and the freshwater species P. aciculiferum, but here we suggest that these two are part of a bigger story about species radiation.…”

“…S. hangoei, known from the Baltic Sea, can grow in salinities up to 30%, while P. aciculiferum is a freshwater species found in lakes (Logares et al, 2007a). Moreover, S. hangoei was shown not to cluster with confirmed Scrippsiella species.…”

“…Moreover, S. hangoei was shown not to cluster with confirmed Scrippsiella species. The two species are morphologically distinct but show no difference in the ribosomal DNA markers traditionally used for species delimitation (Logares et al, 2007a. Later, S. aff.…”

“…A case of recent diversification following the transition from marine to freshwater has been proposed for two species of dinoflagellates, Scrippsiella hangoei and Peridinium aciculiferum (Logares et al, 2007a). S. hangoei, known from the Baltic Sea, can grow in salinities up to 30%, while P. aciculiferum is a freshwater species found in lakes (Logares et al, 2007a).…”