Genetic analyses of Dinophysis spp. support kleptoplastidy

The question of whether the toxin-producing and bloom-forming dinoflagellate genus Dinophysis contains plastids that are permanent or contains temporary so-called kleptoplastids is still unresolved. We sequenced plastid 16S rRNA gene, the complete trnA gene and the intergenic transcribed spacer region located between the trnA gene and the 23S rRNA gene, and performed diagnostic PCR on cells of the genus Dinophysis. Dinophysis spp. were collected from five different geographical regions: the Baltic Sea, the North Sea, the Greenland Sea and the Norwegian fjord Masfjorden. In most cases the sequence analysis showed that the sequences were identical to each other and to sequences from the cryptophyte Teleaulax amphioxeia SCCAP K0434, regardless of the place of sampling or the species analyzed. The exception was some cells of Dinophysis spp. from the Greenland Sea. These contained a 16S rRNA gene sequence that was more closely related to the cryptophyte Geminigera cryophila. The cells of Dinophysis contained either one of the 16S rRNA gene sequences or both in the same cell. Our results challenge the hypothesis that the plastids in Dinophysis are permanent and suggest that they are more likely to be kleptoplastids.     

Molecular evidence for plastid robbery (Kleptoplastidy) in Dinophysis,a dinoflagellate causing diarrhetic shellfish poisoning

The dinoflagellate genus Dinophysis contains species known to cause diarrhetic shellfish poisoning. Although most photosynthetic dinoflagellates have plastids with peridinin, photosynthetic Dinophysis species have cryptophyte-like plastids containing phycobilin rather than peridinin. We sequenced nuclear- and plastid-encoded SSU rDNA from three photosynthetic species of Dinophysis for phylogenetic analyses. In the tree of nuclear SSU rDNA, Dinophysis was a monophyletic group nested with peridinin-containing dinoflagellates. However, in the tree of plastid SSU rDNA, the Dinophysis plastid lineage was within the radiation of cryptophytes and was closely related to Geminigera cryophila. These analyses indicate that an ancestor of Dinophysis, which may have originally possessed peridinin-type plastid and lost it subsequently, adopted a new plastid from a cryptophyte. Unlike dinoflagellates with fully integrated plastids, the Dinophysis plastid SSU rDNA sequences were identical among the three species examined, while there were species-specific base substitutions in their nuclear SSU rDNA sequences. Queries of the DNA database showed that the plastid SSU rDNA sequence of Dinophysis is almost identical to that of an environmental DNA clone of a <10 pm sized plankter, possibly a cryptophyte and a likely source of the Dinophysis plastid. The present findings suggest that these Dinophysis species engulfed and temporarily retained plastids from a cryptophyte.     

psbA based molecular analysis of cross-feeding experiments suggests that Dinophysis acuta does not harbour permanent plastids

Toxic marine dinoflagellate species of the genus Dinophysis Ehrenberg are obligate mixotrophs that require feeding on the ciliate Mesodinium rubrum and light to achieve growth. It is now well known that they harbour plastids of cryptophyte origin, particularly of the genus Teleaulax, Plagioselmis or Geminigera group (TPG clade). Nevertheless, whether these plastids are permanent, or periodically acquired from M. rubrum prey, need additional studies in different phototrophic Dinophysis species. The origin of plastids from Dinophysis acuta Ehrenberg, one of the main agents of diarrhetic shellfish poisoning (DSP) outbreaks in Western Europe, was investigated here. Cross feeding-starvation experiments were carried out with cultures of D. acuta using M. rubrum as prey, the latter fed with two cryptophyte species, Teleaulax amphioxeia Hill and Teleaulax gracilis, belonging to the TPG clade in addition to Falcomonas sp. and Hemiselmis sp. The fate of cryptophyte plastids transferred to D. acuta through its ciliate prey was investigated using the plastid psbA gene as a tracer.     

A novel type of kleptoplastidy in Dinophysis (Dinophyceae): presence of haptophyte-type plastid in Dinophysis mitra

Red-fluorescent, non-phycobilin-containing plastids were found in the heterotrophic dinoflagellate, Dinophysis mitra. Transmission electron microscopy showed that they contained a three-layer thylakoid, the absence of girdle lamella, and an embedded pyrenoid with thylakoid intrusions. These characteristics all coincide with haptophyte plastids. Phylogenetic analysis of the plastid small-subunit ribosomal DNA (SSU rDNA) revealed that the Dinophysis mitra sequences are distantly related to those of phycobilin-containing Dinophysis species and are positioned within a lineage of haptophytes belonging to Prymnesiophyceae. Because the plastid SSU rDNA sequences of Dinophysis mitra showed significant heterogeneity, despite being derived from a single species, it is highly likely that they were not established as plastids through an evolutionary process but are "kleptoplastids" (temporally stolen plastids) from multiple sources of haptophytes in the environment. We deduced that Dinophysis mitra takes up haptophytes myzocytotically and selectively retains the plastid with surrounding plastidal membranes, whereas other haptophyte cell components are degraded. This represents another type of kleptoplastidy in the Dinophysis species, which mostly harbor cryptophyte plastids, and is the first evidence of kleptoplastidy originating from haptophytes.     

Nuclear, mitochondrial and plastid gene phylogenies of Dinophysis miles (Dinophyceae): evidence of variable types of chloroplasts

The Dinophysis genus is an ecologically and evolutionarily important group of marine dinoflagellates, yet their molecular phylogenetic positions and ecological characteristics such as trophic modes remain poorly understood. Here, a population of Dinophysis miles var. indica was sampled from South China Sea in March 2010. Nuclear ribosomal RNA gene (rDNA) SSU, ITS1-5.8S-ITS2 and LSU, mitochondrial genes encoding cytochrome B (cob) and cytochrome C oxidase subunit I (cox1), and plastid rDNA SSU were PCR amplified and sequenced. Phylogenetic analyses based on cob, cox1, and the nuclear rRNA regions showed that D. miles was closely related to D. tripos and D. caudata while distinct from D. acuminata. Along with morphology the LSU and ITS1-5.8S-ITS2 molecular data confirmed that this population was D. miles var. indica. Furthermore, the result demonstrated that ITS1-5.8S-ITS2 fragment was the most effective region to distinguish D. miles from other Dinophysis species. Three distinct types of plastid rDNA sequences were detected, belonging to plastids of a cryptophyte, a haptophyte, and a cyanobacterium, respectively. This is the first documentation of three photosynthetic entities associated with a Dinophysis species. While the cyanobacterial sequence likely represented an ectosymbiont of the D. miles cells, the detection of the cryptophyte and haptophyte plastid sequences indicates that the natural assemblage of D. miles likely retain more than one type of plastids from its prey algae for temporary use in photosynthesis. The result, together with recent findings of plastid types in other Dinophysis species, suggests that more systematic research is required to understand the complex nutritional physiology of this genus of dinoflagellates.     

Fate of green plastids in Dinophysis caudata following ingestion of the benthic ciliate Mesodinium coatsi: Ultrastructure and psbA gene

Phototrophic Dinophysis species are known to acquire plastids of the cryptophyte Teleaulax amphioxeia through feeding on the ciliate Mesodinium rubrum or M. cf. rubrum. In addition, several molecular studies have detected plastid encoding genes of various algal taxa within field populations of Dinophysis species. The trophic pathway by which Dinophysis species acquire plastids from algae other than the cryptophyte genus Teleaulax, however, is unknown. In this study, we examined the fate of prey organelles and plastid genes obtained by Dinophysis caudata through ingestion of Mesodinium coatsi, a benthic ciliate that retains green plastids of Chroomonas sp. Transmission electron microscopy and molecular analysis revealed relatively rapid digestion of prey-derived plastids. Following digestion of M. coatsi, however, photodamaged D. caudata cells having olive-green rather than reddish-brown plastids were able to recover some of their original reddish-brown pigmentation. Results further suggest that plastid genes of various algal taxa detected in field populations of Dinophysis species may reflect prey diversity rather than sequestration of multiple plastid types. Ingestion and digestion of prey other than M. rubrum or M. cf. rubrum may also provide nutritional requirements needed to repair and perhaps maintain sequestered T. amphioxeia plastids.     

Anucleated cryptophyte vestiges in the gonyaulacalean dinoflagellates Amylax buxus and Amylax triacantha (Dinophyceae)

Cryptophyte vestiges showing selective digestion of nuclei were found in the gonyaulacalean dinoflagellates Amylax buxus (Balech) Dodge and Amylax triacantha (Jörgensen) Sournia. They emitted bright yellow‐orange fluorescence (590‐nm emission) under epifluorescent microscopy and possessed U‐shaped plastids, suggesting the vestiges were active in photosynthesis. Under transmission electron microscopy, the plastid was characterized by a loose arrangement of two to three thylakoid stacks and included a stalked pyrenoid, as in the cryptophyte genus Teleaulax. Indeed, molecular data based on the plastid small‐subunit rRNA gene demonstrated that the vestiges in Amylax originated from Teleaulax amphioxeia. The stolen plastid (kleptoplastids) in Dinophysis is also derived from this cryptophyte species. However, in sharp contrast to Dinophysis, the plastid of the vestige in Amylax was surrounded by a double layer of plastid endoplasmic reticulum, and within the periplastidal area, a nucleomorph was retained. The vestiges also possessed mitochondria with characteristic plate‐like cristae, but lost the cell‐surface structure. The phagocytotic membrane of the dinoflagellates seemed to surround the cryptophytes right after the incorporation, but the membrane itself would probably be digested eventually. Remarkably, only one cryptophyte cell among 14 vestiges in a cell of A. buxus had a nucleus. This is the first recording of possible kleptoplastidy in gonyaulacalean dinoflagellates, and documents the strategy of a dinoflagellate involving the selective elimination of the cryptophyte nucleus.     

Plastid genome sequence of the cryptophyte alga Rhodomonas salina CCMP1319: lateral transfer of putative DNA replication machinery and a test of chromist plastid phylogeny

Cryptophytes are a group of unicellular algae with chlorophyll c-containing plastids derived from the uptake of a secondary (i.e., eukaryotic) endosymbiont. Biochemical and molecular data indicate that cryptophyte plastids are derived from red algae, yet the question of whether or not cryptophytes acquired their red algal plastids independent of those in heterokont, haptophyte, and dinoflagellate algae is of long-standing debate. To better understand the origin and evolution of the cryptophyte plastid, we have sequenced the plastid genome of Rhodomonas salina CCMP1319: at 135,854 bp, it is the largest secondary plastid genome characterized thus far. It also possesses interesting features not seen in the distantly related cryptophyte Guillardia theta or in other red secondary plastids, including pseudogenes, introns, and a bacterial-derived gene for the tau/gamma subunit of DNA polymerase III (dnaX), the first time putative DNA replication machinery has been found encoded in any plastid genome. Phylogenetic analyses indicate that dnaX was acquired by lateral gene transfer (LGT) in an ancestor of Rhodomonas, most likely from a firmicute bacterium. A phylogenomic survey revealed no additional cases of LGT, beyond a noncyanobacterial type rpl36 gene similar to that recently characterized in other cryptophytes and haptophytes. Rigorous concatenated analysis of 45 proteins encoded in 15 complete plastid genomes produced trees in which the heterokont, haptophyte, and cryptophyte (i.e., chromist) plastids were monophyletic, and heterokonts and haptophytes were each other's closest relatives. However, statistical support for chromist monophyly disappears when amino acids are recoded according to their chemical properties in order to minimize the impact of composition bias, and a significant fraction of the concatenate appears consistent with a sister-group relationship between cryptophyte and haptophyte plastids.     

Cyanobacterial endosymbionts in the benthic dinoflagellate Sinophysis canaliculata (Dinophysiales, Dinophyceae)

Photosynthetic dinoflagellates possess a great diversity of plastids that have been acquired through successful serial endosymbiosis. The peridinin-containing plastid in dinoflagellates is canonical, but many other types are known within this group. Within the Dinophysiales, several species of Dinophysis contain plastids, derived from cryptophytes or haptophytes. In this work, the presence of numerous intracellular cyanobacteria-like microorganisms compartmentalized by a separate membrane is reported for the first time within the benthic dinophysoid dinoflagellate Sinophysis canaliculata Quod et al., a species from a genus morphologically close to Dinophysis. Although the contribution of these cyanobacterial endosymbionts to S. canaliculata is still unknown, this finding suggests a possible undergoing primary endosymbiosis in a dinoflagellate.     

Diversity and plastid types in Dinophysis acuminata complex (Dinophyceae) in Scottish waters

Dinophysis acuminata produces lipophilic shellfish toxins (LSTs) that have economic and ecological impact on marine invertebrates in NE Atlantic where aquaculture farming is prevalent. Identification of D. acuminata can be complex. Cells exhibit a variety of morphotypes that overlap between species making identification using routine light microscopy difficult. These cells are mixotrophic and their population size is influenced by hydrographic conditions and prey populations. Dinophysis cells are able to acquire and temporarily keep prey plastids from a variety of photosynthetic unicellular sources. The Dinophysis community in Scottish waters tend to be dominated by cells with morphologies that appear to be variants of D. acuminata/norvegica complex particularly during late spring/early summer. To determine the identity of these morphotypes, DNA barcoding was performed on 32 single cell isolates from sites around the Scottish coast using the ribosomal internal transcribed spacer 1 (ITS1) and a partial cytochrome oxidase I (COI) fragment on the same single cells. Although the cells exhibited a variety of morphotypes, most were restricted to one cluster containing D. acuminata and three grouped with Dinophysis ovum. This is the first molecular confirmation of the presence of D. ovum in Scottish waters. Two isolates showed considerable divergence – one was unidentifiable from the public databases, whilst the other matched a Dinophysis cf. acuta isolate from Canada. To investigate prey plastids, molecular analysis of these Dinophysis single cells was conducted with a partial fragment of the plastid ribosomal marker (16S). Most cells harboured plastids from the cryptophyte Teleaulax – the most commonly reported plastid type, however one cell harboured a Rhodomonas/Storeatula derived plastid. This finding increases the range and variety of cryptophyte plastids found in Dinophysis and increases the range of prey-types.     

Phylogeny of Dinoflagellate Plastid Genes Recently Transferred to the Nucleus Supports a Common Ancestry with Red Algal Plastid Genes

It is generally accepted that peridinin-containing dinoflagellate plastids are derived from red alga, but whether they are secondary plastids equivalent to plastids of stramenopiles, haptophytes, or cryptophytes, or are tertiary plastids derived from one of the other secondary plastids, has not yet been completely resolved. As secondary plastids, plastid gene phylogeny should mirror that of nuclear genes, while incongruence in the two phylogenies should be anticipated if their origin was as tertiary plastids. We have analyzed the phylogeny of plastid-encoded genes from Lingulodinium as well as that of nuclear-encoded dinoflagellate homologues of plastid-encoded genes conserved in all other plastid genome sequences. Our analyses place the dinoflagellate, stramenopile, haptophyte, and cryptophyte plastids firmly in the red algal lineage, and in particular, the close relationship between stramenopile plastid genes and their dinoflagellate nuclear-encoded homologues is consistent with the hypothesis that red algal-type plastids have arisen only once in evolution.     

Selective feeding and foreign plastid retention in an Antarctic dinoflagellate

The peridinin‐containing plastid found in most photosynthetic dinoflagellates is thought to have been replaced in a few lineages by plastids of chlorophyte, diatom, or haptophyte origin. Other distinct lineages of phagotrophic dinoflagellates retain functional plastids obtained from algal prey for different durations and with varying source species specificity. 18S rRNA gene sequence analyses have placed a novel gymnodinoid dinoflagellate isolated from the Ross Sea (RSD) in the Kareniaceae, a family of dinoflagellates with permanent plastids of haptophyte origin. In contrast to other species in this family, the RSD contains kleptoplastids sequestered from its prey, Phaeocystis antarctica. Culture experiments were employed to determine whether the RSD fed selectively on P. antarctica when offered in combination with another polar haptophyte or cryptophyte species, and whether the RSD, isolated from its prey and starved, would take up plastids from P. antarctica or from other polar haptophyte or cryptophyte species. Evidence was obtained for selective feeding on P. antarctica, plastid uptake from P. antarctica, and increased RSD growth in the presence of P. antarctica. The presence of a peduncle‐like structure in the RSD suggests that kleptoplasts are obtained by myzocytosis. RSD cells incubated without P. antarctica were capable of survival for at least 29.5 months. This remarkable longevity of the RSD's kleptoplasts and its species specificity for prey and plastid source is consistent with its prolonged co‐evolution with P. antarctica. It may also reflect the presence of a plastid protein import mechanism and genes transferred to the dinokaryon from a lost permanent haptophyte plastid.     

THE EVOLUTION OF RNA POLYMERASE II IN RED ALGAE

Cryptophytes are photosynthetic protists that have acquired their plastids through the secondary symbiotic uptake of a red alga. A remarkable feature of cryptophytes is that they maintain a reduced form of the red algal nucleus, the nucleomorph, between the second and third plastid membranes (periplastidial compartment, PC). The nucleomorph is thought to be a transition state in the evolution of secondary plastids with this genome ultimately being lost (e.g., as in heterokonts, haptophytes, euglenophytes) when photosynthesis comes under full control of the "host" nucleus. For this to happen, all genes for plastid function must be transferred from the nucleomorph to the nucleus. In this regard, it is generally assumed that nucleomorph genes with functions unrelated to plastid or PC maintenance are lost. Surprisingly, we show here the existence of a novel type of actin gene in the host nucleus of the cryptophyte, Pyrenomonas helgolandii , that has originated from the nucleomorph genome of the symbiont. Our results demonstrate for the first time that secondary symbionts can contribute genes to the host lineage that are unrelated to plastid function. These genes are akin to the products of gene duplication and provide a source of evolutionary novelty that could significantly increase the genetic diversity of the host lineage. We postulate that this may be a common phenomenon in algae containing secondary plastids that has yet to be fully appreciated due to a dearth of evolutionary studies of nuclear genes in these taxa.     

SYMBIOTIC ORIGIN OF A NOVEL ACTIN GENE IN THE CRYPTOPHYTE,PYRENOMONAS HELGOLANDII

Cryptophytes are photosynthetic protists that have acquired their plastids through the secondary symbiotic uptake of a red alga. A remarkable feature of cryptophytes is that they maintain a reduced form of the red algal nucleus, the nucleomorph, between the second and third plastid membranes (periplastidial compartment, PC). The nucleomorph is thought to be a transition state in the evolution of secondary plastids with this genome ultimately being lost (e.g., as in heterokonts, haptophytes, euglenophytes) when photosynthesis comes under full control of the “host” nucleus. For this to happen, all genes for plastid function must be transferred from the nucleomorph to the nucleus. In this regard, it is generally assumed that nucleomorph genes with functions unrelated to plastid or PC maintenance are lost. Surprisingly, we show here the existence of a novel type of actin gene in the host nucleus of the cryptophyte, Pyrenomonas helgolandii, that has originated from the nucleomorph genome of the symbiont. Our results demonstrate for the first time that secondary symbionts can contribute genes to the host lineage that are unrelated to plastid function. These genes are akin to the products of gene duplication and provide a source of evolutionary novelty that could significantly increase the genetic diversity of the host lineage. We postulate that this may be a common phenomenon in algae containing secondary plastids that has yet to be fully appreciated due to a dearth of evolutionary studies of nuclear genes in these taxa.     

The origins of plastids

A new theory of plastid origins is presented in which only two symbiotic events are needed to explain the origin of the six fundamentally different types of plastid, which all probably originated in anteriorly biciliated phagotrophic cells. Four of them can be derived directly from a single endosymbiotic cyanophyte by the independent loss of different cyanophyte characters and the evolution of new characters in the immediate descendants of this primary endosymbiosis. Retention of the phagosomal membrane as well as the prokaryotic plasma and outer membrane could produce the dinozoan and euglenid plastids with three envelope membranes, whereas the loss of the phagosomal membrane could produce the two-membraned envelopes characteristic of the Biliphyta and Verdiplantae*. The phycobilins were retained essentially unaltered in the Biliphyta, but are modified or lost in the other lines. In the ancestor of the Euglenozoa and Verdiplantae they were replaced by chlorophyll b. In the ancestor of algae possessing chlorophyll c they were modified to the cryptophyte type, concomitantly with the evolution of chlorophyll c₂: one line of descent from this ancestor produced the dinozoan plastid by the complete loss of phycobilins, while the other was incorporated by endosymbiosis into another phagotrophic bibiliate to produce the cryptophyte plastid. The latter evolved into the chromophyte plastid by the loss of phycobilins and the evolution of chlorophyll c₂. The conversion of the endosymbiont into a plastid depended on the evolution of a system to transport proteins into it. I argue that this occurred by the modification of the pre-existing mitochondrial transport system, and that the major modifications needed to adjust this to plastids with more than two envelope membranes led to evolution of a new tubular or disc-like morphology for the mitochondrial cristae of these groups. This new cristal morphology is maintained by stabilizing selection even in species that have secondarily lost plastids.     

Eukaryote-eukaryote endosymbioses: insights from studies of a cryptomonad alga.

It has been proposed that those plants which contain photosynthetic plastids surrounded by more than two membranes have arisen through secondary endosymbiotic events. Molecular evidence confirms this proposal, but the nature of the endosymbiont(s) and the number of endosymbioses remain unresolved. Whether plastids arose from one type of prokaryotic ancestor or multiple types is the subject of some controversy. In order to try to resolve this question, the plastid gene content and arrangement has been studied from a cryptomonad alga. Most of the gene clusters common to photosynthetic prokaryotes and plastids are preserved and seventeen genes which are not found on the plastid genomes of land plants have been found. Together with previously published phylogenetic analyses of plastid genes, the present data support the notion that the type of prokaryote involved in the initial endosymbiosis was from within the cyanobacterial assemblage and that an early divergence giving rise to the green plant lineage and the rhodophyte lineage resulted in the differences in plastid gene content and sequence between these two groups. Multiple secondary endosymbiotic events involving a eukaryotic (probably rhodophytic alga) and different hosts are hypothesized to have occurred subsequently, giving rise to the chromophyte, cryptophyte and euglenophyte lineages.     

Symbiotic origin of a novel actin gene in the cryptophyte Pyrenomonas helgolandii

Cryptophytes are photosynthetic protists that have acquired their plastids through the secondary symbiotic uptake of a red alga. A remarkable feature of cryptophytes is that they maintain a reduced form of the red algal nucleus, the nucleomorph, between the second and third plastid membranes (periplastidial compartment; PC). The nucleomorph is thought to be a transition state in the evolution of secondary plastids, with this genome ultimately being lost when photosynthesis comes under full control of the "host" nucleus (e.g., as in heterokonts, haptophytes, and euglenophytes). Genes presently found in the nucleomorph seem to be restricted to those involved in its own maintenance and to that of the plastid; other genes were lost as the endosymbiont was progressively reduced to its present state. Surprisingly, we found that the cryptophyte Pyrenomonas helgolandii possesses a novel type of actin gene that originated from the nucleomorph genome of the symbiont. Our results demonstrate for the first time that secondary symbionts can contribute genes to the host lineage which are unrelated to plastid function. These genes are akin to the products of gene duplication or lateral transfer and provide a source of evolutionary novelty that can significantly increase the genetic diversity of the host lineage. We postulate that this may be a common phenomenon in algae containing secondary plastids that has yet to be fully appreciated due to a dearth of evolutionary studies of nuclear genes in these taxa.     

Acquired phototrophy in ciliates: a review of cellular interactions and structural adaptations

Many ciliates acquire the capacity for photosynthesis through stealing plastids or harboring intact endosymbiotic algae. Both phenomena are a form of mixotrophy and are widespread among ciliates. Mixotrophic ciliates may be abundant in freshwater and marine ecosystems, sometimes making substantial contributions toward community primary productivity. While mixotrophic ciliates utilize phagotrophy to capture algal cells, their endomembrane system has evolved to partially bypass typical heterotrophic digestion pathways, enabling metabolic interaction with foreign cells or organelles. Unique adaptations may also be found in certain algal endosymbionts, facilitating establishment of symbiosis and nutritional interactions, while reducing their fitness for survival as free-living cells. Plastid retaining oligotrich ciliates possess little selectivity from which algae they sequester plastids, resulting in unstable kleptoplastids that require frequent ingestion of algal cells to replace them. Mesodinium rubrum (=Myrionecta rubra) possesses cryptophyte organelles that resemble a reduced endosymbont, and is the only ciliate capable of functional phototrophy and plastid division. Certain strains of M. rubrum may have a stable association with their cryptophyte organelles, while others need to acquire a cryptophyte nucleus through feeding. This process of stealing a nucleus, termed karyoklepty, was first described in M. rubrum and may be an evolutionary precursor to a stable, reduced endosymbiont, and perhaps eventually a tertiary plastid. The newly described Mesodinium"chamaeleon," however, is less selective of which cryptophyte species it will retain organelles, and appears less capable of sustained phototrophy. Ciliates likely stem from a phototrophic ancestry, which may explain their propensity to practice acquired phototrophy.     

Ribosomal DNA phylogeny of the Bangiophycidae (Rhodophyta) and the origin of secondary plastids

We sequenced the nuclear small subunit ribosomal DNA coding region from 20 members of the Bangiophycidae and from two members of the Florideophycidae to gain insights into red algal evolution. A combined alignment of nuclear and plastid small subunit rDNA and a data set of Rubisco protein sequences were also studied to complement the understanding of bangiophyte phylogeny and to address red algal secondary symbiosis. Our results are consistent with a monophyletic origin of the Florideophycidae, which form a sister-group to the Bangiales. Bangiales monophyly is strongly supported, although Porphyra is polyphyletic within Bangia. Bangiophycidae orders such as the Porphyridiales are distributed over three independent red algal lineages. The Compsopogonales sensu stricto, consisting of two freshwater families, Compsopogonaceae and Boldiaceae, forms a well-supported monophyletic grouping. The single taxon within the Rhodochaetales, Rhodochaete parvula, is positioned within a cluster containing members of the Erythropeltidales. Analyses of Rubisco sequences show that the plastids of the heterokonts are most closely related to members of the Cyanidiales and are not directly related to cryptophyte and haptophyte plastid genomes. Our results support the independent origins of these secondary algal plastids from different members of the Bangiophycidae.