Genetic identity of free‐living Symbiodinium obtained over a broad latitudinal range in the Japanese coast

Abstract

Summary The dinoflagellate Symbiodinium is well known to engage symbiosis with various marine animals, including corals. Recent records of environmental Symbiodinium (occurring in the environment and separately from host animals; usually referred to as ‘free‐living’ Symbiodinium) are of special interest, since these environmental populations are essential as symbiont sources for many host animals. In the present study, we carried out a phylogenetic analysis of environmental Symbiodinium isolates (culture strains) from sand, tide pools, or macroalgal surfaces, and environmental DNA clones extracted from the water‐column, at numerous sites around Japan. Our phylogenetic analysis based on the nuclear rRNA gene (internal transcribed spacers ‐1, ‐2, and 5.8S), indicated that most of the environmental isolates form monophyletic subclades within the Clade‐A lineage, and separate from a host‐associated Clade‐A population with high bootstrap values. Results of the partial nuclear 28S rDNA phylogeny and thecal‐plate observations revealed that these environmental isolates were closely related to a previously‐described ‘planktonic species’, Symbiodinium natans Gert Hansen et Daugbjerg, which was isolated from a plankton‐net sample from the Northeast‐Atlantic Ocean. On the other hand, the environmental DNA clones were also noted to be mostly nested within host‐associated Symbiodinium groups scattered in various clades. These results led to the assumption that the environmental Symbiodinium can be divided into two groups. One group, as typified by environmental isolates in the present study and previous reports, may be exclusively free‐living; the other group exists transiently in free‐living forms, possibly having been expelled from animal hosts. The populations within the latter group probably represent environmental sources of viable symbionts, because these are normally host‐associated. However, the Symbiodinium in the former group are not expected to engage in stable symbioses with host cnidarians.

The free-living Symbiodinium reservoir and scleractinian coral symbiont acquisition

“…Sediment can also serve as a holding habitat and reservoir for the resting (or dormant) stages of benthic microalgae, especially for dinoflagellates (Dale 1976;Baldwin 1987;Lewis et al 1999). A number of studies have now identified free-living Symbiodinium in the sediment as a constituent of the MPB (Carlos et al 1999;Hirose et al 2008;Littman et al 2008;Reimer et al 2010;Takabayashi et al 2012;Yamashita and Koike 2013). Additionally, symbiont acquisition during exposure to sediment was reported by Adams et al (2009) and Cumbo et al (2013), demonstrating…”

“…There are at least seven other formally described species in the genus, and at least eight other species that have been referred to without formal description (see LaJeunesse et al (2012)). It is likely that many new species will be discovered, especially in view of the uncharacterised diversity of Symbiodinium types that exists exclusively outside of hosts (Yamashita and Koike 2013).…”

“…In contrast, empirical data for population dynamics, distribution, and physiology of free-living Symbiodinium are limited. 'Freeliving' (FL) refers to either: A) living outside a host while retaining the facility of forming symbioses (Hirose et al 2008), and this term includes 'transiently free-living' (TFL) cells recently expelled from their hosts that may not continuously persist in a free-living state (Yamashita and Koike 2013); or B)…”

“…Indeed, a number of studies have now identified free-living Symbiodinium cells in reef sand/sediment (Carlos et al 1999;Hirose et al 2008;Littman et al 2008;Reimer et al 2010;Takabayashi et al 2012;Yamashita and Koike 2013). Moreover, juvenile corals are able to acquire a consortium of symbionts through exposure to sediment (Adams et al 2009;Cumbo et al 2013).…”

“…Littman et al (2008) Takabayashi et al 2012;Yamashita and Koike 2013;Nitschke et al 2015). Investigating the dynamics and potential source populations of free-living Symbiodinium is required to begin differentiating between these categories.…”