One-year survey of a single Micronesian reef reveals extraordinarily rich diversity of Symbiodinium types in soritid foraminifera

Abstract

Recent molecular studies of symbiotic dinoXagellates (genus Symbiodinium) from a wide array of invertebrate hosts have revealed exceptional Wne-scale symbiont diversity whose distribution among hosts, regions and environments exhibits signiWcant biogeographic, ecological and evolutionary patterns. Here, similar molecular approaches using the internal transcribed spacer-2 (ITS-2) region were applied to investigate cryptic diversity in Symbiodinium inhabiting soritid foraminifera. Approximately 1,000 soritid specimens were collected and examined during a 12-month period over a 40 m depth gradient from a single reef in Guam, Micronesia. Out of 61 ITS-2 types distinguished, 46 were novel. Most types found are speciWc for soritid hosts, except for three types (C1, C15 and C19) that are common in metazoan hosts. The distribution of these symbionts was compared with the phylotype of their foraminiferal hosts, based on soritid small subunit ribosomal DNA sequences, and three new phylotypes of soritid hosts were identiWed based on these sequences. Phylogenetic analyses of 645 host-symbiont pairings revealed that most Symbiodinium types associated speciWcally with a particular foraminiferal host genus or species, and that the genetic diversity of these symbiont types was positively correlated with the genetic diversity found within each of the three host genera. Compared to previous molecular studies of Symbiodinium from other locations worldwide, the diversity reported here is exceptional and suggests that Micronesian coral reefs are home to a remarkably large Symbiodinium assemblage.

The distribution of Symbiodinium diversity within individual host foraminifera

“…They host a more genetically diverse assortment of symbiont types than most coral species (Pochon et al 2007), supporting a hypothesis that they may be a reservoir for Symbiodinium diversity in the reef community. While most Symbiodinium hosts, such as corals, clams, and sponges feed primarily from the seawater flowing over a reef, foraminifera feed directly from the surface upon which they live (see video in electronic supplementary material), and thus may directly interact with the benthic Symbiodinium community.…”

“…In order to identify and name the ancestral haplotypes, their ITS2 sequences were aligned (using MUSCLE) to those sequences found in Pochon et al (2007), wherein the most fine scale diversity of ITS2 types to date has been described. Pairwise distance to the closest match sequence was calculated to quantify homology.…”

“…2). In an earlier study of 1,010 different individual foraminifera from Guam, a high diversity of Symbiodinium ITS2 types from DGGE bands was found, with 61 different types from five different clades (Pochon et al 2007). Though diversity of cloned PCR products and diversity of DGGE bands are not directly comparable, populations of foraminifera from Guam and PNG both harbor a diverse array of symbionts.…”

“…2); the clones have many single base-pair differences, likely an artifact of either intragenomic variation or PCR mutations. Since ecologically distinct ITS2 haplotypes can be separated by only a few base-pair changes Sampayo et al 2009), grouping diverse Symbiodinium ITS-region haplotypes into statistical parsimony networks using TCS is a method that conservatively forms groups which are ecologically distinct (Rodriguez-Lanetty 2003;RodriguezLanetty et al 2006b;Pochon et al 2007;Correa and Baker 2009). …”

“…Since then, Xavier Pochon and his colleagues have described in detail the genetic diversity of Symbiodinium found in these foraminifera (reviewed in Pochon and Pawlowski 2006), examining factors such as host specificity (Pochon et al 2001;Garcia-Cuetos et al 2005), biogeographic distribution (Pochon et al 2004), and local ecology (Pochon et al 2007). Analysis of Symbiodinium from foraminifera using DGGE indicates that 15% of samples from Guam had mixed symbiont types (Pochon et al 2007), but an explicit study of symbiont heterogeneity in foraminifera has, until now, not been done. Thus, the first aim of this study was to examine more closely the symbiont composition within individual foraminifera.…”