Molecular systematics of Foraminifera

Foraminifera, affectionately called "forams", are classically defined as a group of protists having tectinous, agglutinated or calcareous shells (tests) and inhabiting marine or brackish water environments. Our molecular study, however, shows that a naked "giant freshwater amoeba" Reticulomyxa filosa is actually a foraminiferan.



The foraminiferal tests deposited in the sediments since 550 millions years form the most important group of microfossils, widely used in biostratigraphy and paleoenvironmental reconstructions. The paleontological data, however, yield no evidence concerning the foraminiferal origin. A lack of shared morphologic features between foraminifera and other protists makes phylogenetic placement of this group even more difficult.

The first attempts to investigate the origin of foraminifera based on molecular data gave conflicting results. The phylogenetic analysis of partial sequences of the LSU rDNA have shown that foraminifera branch close to slime molds (Dictyostelium, Physarum) and Entamoeba in the eukaryotic tree (Pawlowski et al., 1994). However, on the basis of two SSU rDNA sequences, Wray et al. (1995) placed the foraminifera within the assemblage of Alveolata, as a sister group to the ciliates. Since the respective positions of alveolates and slime molds are well conserved in both SSU and LSU rRNA trees, it was obvious that in one case, PCR-amplified sequences have been erroneously attributed to the foraminifera.

Several complete and partial SSU rDNA sequences of benthic and planktonic foraminifera confirmed later the LSU rDNA tree topology (Pawlowski et al., 1996; Darling et al. 1996, Wade et al. 1996). Phylogenetic analysis of these sequences, compared to those of other unicellular eukaryotes, place the foraminifera in the lower part of the eukaryotic tree, between the amitochondriate Diplomonads and Euglenozoa, i.e. even deeper than in the LSU rDNA tree. In both LSU and SSU rRNA trees, the branch separating foraminifera from the upper part of the tree is associated with a bootstrap score of 100%, making unlikely their origin within the clade of alveolates as proposed by Wray et al. (1995).

According to ribosomal sequence data, the foraminifera diverged early in the evolution of eukaryotes, among the earliest mitochondriate lineages. Such early origin, however, contrasts with relatively late appearance of the first fossil foraminifera (about 550 millions years ago) and with several highly evolved characters that these organisms possess. It is probable, that foraminifera have evolved from some ancestral lineage that did not form tests and therefore was not preserved in the fossil record. This hypothesis was recently confirmed by our study of a naked foram Reticulomyxa filosa (Pawlowski et al. 1999a, 1999b). Alternatively, the position of foraminifera in the rRNA trees is biased by very rapid rates of rRNA evolution in these organisms that produce an artificial grouping of foraminifera with early evolved protists lineages.

people working on this subject: David LONGET, Delia FONTAINE, Jan Wojciech PAWLOWSKI, Jacqueline GUIARD, Yurika UJIIE, Béatrice LECROQ, Loïc PILLET, Michaël CID.