Molecular Identification of Algal Endosymbionts in Large Miliolid Foraminifera: 1. Chlorophytes

Large miliolid foraminifers bear various types of algal endosymbionts including chlorophytes, dinoflagellates, rhodophytes, and diatoms. Symbiosis plays a key role in the adaptation of large foraminifera to survival and growth in oligotrophic seas. The identity and diversity of foraminiferal symbionts, however, remain largely unknown. In the present work we use ribosomal DNA (rDNA) sequences to identify chlorophyte endosymbionts in large miliolid foraminifera of the superfamily Soritacea. Partial 18S and complete Internal Transcribed Spacer (ITS) rDNA sequences were obtained from symbionts of eight species representing all genera of extant chlorophyte-bearing Soritacea. Phylogenetic analysis of the sequences confirms the previous fine structure-based identification of these endosymbionts as belonging to the genus Chlamydomonas. All foraminiferal symbionts form a monophyletic group closely related to Chlamydomonas noctigama. The group is composed of seven types identified in this study, including one previously morphologically described species, Chlamydomonas hedleyi. Each of these types can be considered as a separate species, based on the comparison of genetic differences observed between other established Chlamydomonas species. Several foraminiferal species share the same symbiont type, but only one species, Archaias angulatus, was found to bear more than one type.     

Molecular Identification of Algal Endosymbionts in Large Miliolid Foraminifera: 2. Dinoflagellates

Large miliolid foraminifers of the subfamily Soritinae bear symbiotic dinoflagellates morphologically similar to the species of the "Symbiodinium" complex, commonly found in corals and other marine invertebrates. Soritid foraminifers are abundant in coral reefs and it has been proposed that they share their symbionts with other dinoflagellate-bearing reef dwellers. In order to test this hypothesis, we have analysed partial large subunit ribosomal DNA sequences from dinoflagellates symbionts obtained from 28 foraminiferal specimens, and compared them to the corresponding sequences of Symbiodinium-like endosymbionts from various groups of invertebrates. Phylogenetic analysis of our data shows that all soritid symbionts belong to the "Symbiodinium" species complex, within which they form seven different molecular types (Frl-Fr7). Only one of these types (Fr1) branches within a group of invertebrate symbionts, previously described as type C. The remaining six types form sister groups to coral symbionts previously designed as types B, C, and D. Our data indicate a high genetic diversity and specificity of Symbiodinium-like symbionts in soritids. Except for type C, we have found no evidence for the transmission of symbionts between foraminifers and other symbiont-bearing invertebrates from the same localities. However, exchanges must have occurred frequently between the different species of Soritinae, as suggested by the lack of host specificity and some biogeographical patterns observed in symbiont distribution. Our data suggest that members of the subfamily Soritinae acquired their symbionts at least three times during their history, each acquisition being followed by a rapid diversification and independent radiation of symbionts within the foraminiferal hosts.     

Molecular evidence for host-symbiont specificity in soritid foraminifera

Symbiosis between the dinoflagellate genus Symbiodinium and various invertebrates and protists is an ubiquitous phenomenon in shallow tropical and subtropical waters. Molecular studies undertaken on cnidarian symbionts revealed the presence of several distinctive lineages or subgeneric clades of Symbiodinium whose taxonomic level provides limited information about the specificity between invertebrate hosts and their symbionts. This contrasts with the finding of several Symbiodinium clades being present almost exclusively in foraminifera and belonging to the subfamily Soritinae. To test whether such specificity also exists at a lower taxonomic level within Soritinae, we obtained the SSU rDNA sequences from 159 soritid individuals collected in nine localities worldwide and representing all known morphospecies of this subfamily. For each individual, the symbionts were determined either by sequencing or by RFLP analysis. We distinguished 22 phylotypes of Soritinae in relation with a number of symbiont "groups" corresponding to 3 clades and 5 subclades of Symbiodinium. Among the 22 soritid phylotypes, 14 show strict symbiont specificity and only one was found to be a host for more than two "groups" of Symbiodinium. It is suggested that the strong host-symbiont specificity observed in Soritinae is a combined effect of a selective recognition mechanism, vertical transmission of symbionts, and biogeographical isolation.