Distribution and genetic diversity of the toxic benthic dinoflagellate genus Ostreopsis in Korea

Highlights

• Ostreopsis sp. 1 and sp. 6 were the only Ostreopsis species found in Korea.

• The significant genetic differentiation of a total of 141 Ostreopsis sp.1 isolates from Korea was detected.

• Only the Jeju Island Ostreopsis sp. 1 populations showed a signal in agreement with population equilibrium.

Abstract

Species belonging to the toxic dinoflagellate genus Ostreopsis are widespread, occurring from tropical to temperate waters. As mainly benthic/epiphytic species, they would be expected to show distinct geographical patterns. In this study, ribosomal DNA (rDNA) sequences from partial nuclear LSU D8-D10, 5.8S, and ITS regions were determined for 169 isolates of Ostreopsis species collected from three coastal sites (i.e., Jeju Island, Chuja Island, and Pohang) within Korea. The phylogenetic tree inferred from the LSU rDNA D8-D10 sequences showed that Korean Ostreopsis species corresponded to either Ostreopsis sp. 1 or sp. 6, with Ostreopsis sp. 1 being relatively predominant regarding their distribution. While Ostreopsis sp. 1 occurred throughout all the three sampling sites within Korea, Ostreopsis sp. 6 was confined to the northern part of Jeju Island. When further investigated, the genetic diversity of Ostreopsis sp. 1 in Korea based on ITS sequences showed a total of 21 haplotypes. The presumed ancestral haplotype H3, was also present in the Japanese and Russian populations of Ostreopsis sp. 1. Although the overall demographic history of all the Korean populations of Ostreopsis sp. 1 could not be clearly identified, probably due to a mixture of different regional demographic patterns within Korea, each Ostreopsis sp. 1 population showed a characteristic demographic pattern at a regional scale. While the Jeju Island Ostreopsis sp. 1 population showed a signal in agreement with population equilibrium, the Chuja Island and Pohang Ostreopsis sp. 1 populations showed distribution patterns that are expected in a sudden population expansion model. The results from this study provide a basis for a better understanding of the distribution and genetic structure of the Asian Ostreopsis sp. 1 populations.

Introduction

The population genetic structure of a species in a given area is the outcome of either long-term evolutionary responses, short-term rapid responses to environmental conditions, or both (Shankle et al., 2004; Pyenson and Lindberg, 2011; Hu et al., 2015). Genetic differentiation is considered to be the foundation of ecology and evolution, combining both demographic and genetic processes, including mutation, genetic drift, natural selection, and gene flow (Slatkin, 1993; Roderick, 1996; Amos and Harwood, 1998). These genetic processes result in the genetic differentiation of local populations, whereas gene flow represents a constraint on local genetic differentiation and the adaptation between populations (Slatkin, 1993). While the genetic structure of the population could show the total intraspecific genetic variation and distribution patterns among populations, the roles of multiple factors influencing the phylogeographic patterns of species remain poorly unresolved (Yuan et al., 2011).

The dispersal of marine plankton is known to be affected by numerous atmospheric and oceanographic parameters (e.g., wind, waves, and currents; Palumbi, 2003; Smayda, 2007). Finlay (2002) reported that while species with sizes < 1 mm may be dispersed worldwide, large-size species are restricted by geographical barriers. Nonetheless, phylogeographic studies have shown that some marine phytoplankton (e.g., the dinoflagellate genus Alexandrium and diatom Skeletonema costatum) show geographic differentiation (Scholin et al., 1994; Lilly et al., 2007; Kooistra et al., 2008; Penna et al., 2008).

Marine benthic/epiphytic dinoflagellates include a number of toxic genera such as Gambierdiscus, Coolia, Prorocentrum, and Ostreopsis (Penna et al., 2005; Aligizaki and Nikolaidis, 2006; Parsons et al., 2012). These taxa have been found in the water column as well as in various habitats, such as macroalgae and hard substrates (e.g., rocks, sand, and mollusk shells; Schmidt, 1901; Faust et al., 1996; Vila et al., 2001; Laza-Martinez et al., 2011). Because benthic/epiphytic dinoflagellates have limited capabilities for dispersal, they are expected to show more distinct geographical distribution patterns than those of their marine planktonic relatives. Indeed, several studies (e.g., Leaw et al., 2001; Penna et al., 2010; Sato et al., 2011; Nishimura et al., 2013; Efimova et al., 2014; Leaw et al., 2016) have reported phylogeographic patterns of marine benthic/epiphytic dinoflagellates. For example, the two benthic harmful species Coolia malayensis and C. monotis, are distinguished based on their nuclear LSU and ITS2 sequences and the ITS2 secondary structure information and present distinct geographical distribution (Leaw et al., 2016).

An initial phylogeographic study of the genus Ostreopsis was reported by Leaw et al. (2001). By analyzing their ITS and 5.8S regions of rDNA sequences, the authors showed that Malaysian O. ovata comprised a Malacca Strait clade and a South China Sea clade, with a high level of sequence divergence between them. Since then, other phylogeographic studies on Ostreopsis have mainly focused on O. ovata, which is the most intensively studied species within the genus, and most have been carried out on Mediterranean, Atlantic, South Pacific and Japan (Leaw et al., 2001; Penna et al., 2005, 2010; Laza-Martinez et al., 2011; Sato et al., 2011). Despite reports of the occurrence of Ostreopsis species in Hawaii, Japan, and Russia (Parsons and Preskitt, 2007; Rhodes, 2011; Sato et al., 2011; Efimova et al., 2014), a phylogeographic study of the Asian Ostreopsis species except for the one from Japan has not been widely done yet. In Korea, some studies (Kim et al., 2011; Baek, 2012; Kang et al., 2013; Lee and Park, 2018) have shown the occurrence, abundance, seasonal dynamics, and mixotrophy of Ostreopsis spp. in Korean coastal waters. However, these studies did not aim to study the intra-population or inter-population genetic variability of Ostreopsis species, and thus, they are not enough in order to explain the genetic structure and connectivity among global populations of Ostreopsis.

The present study aimed to (1) identify the Korean Ostreopsis spp. by molecular analysis based on LSU D8-D10 and ITS sequence data; (2) investigate the genetic diversity of Ostreopsis sp. 1 occurring in Korea, as well as its population genetic structure and/or connectivity among Korea-adjacent countries (i.e., Korea, Japan, and Russia) using ITS sequences; and (3) explore whether Korean Ostreopsis sp. 1 population are under population equilibrium or expansion.