Red Algal Parasites Research Articles

Gene-rich plastid genomes of two parasitic red algal species, Laurencia australis and L. verruciformis (Rhodomelaceae, Ceramiales), and a taxonomic revision ofJanczewskia.

Parasitic red algae are an interesting system for investigating the genetic changes that occur in parasites. These parasites have evolved independently multiple times within the red algae. The functional loss of plastid genomes can be investigated in these multiple independent examples, and fine-scale patterns may be discerned. The only plastid genomes from red algal parasites known so far are highly reduced and missing almost all photosynthetic genes. Our study assembled and annotated plastid genomes from the parasites Janczewskia tasmanica and its two Laurencia host species (Laurencia elata and one unidentified Laurencia sp. A25) from Australia and Janczewskia verruciformis, its host species (Laurencia catarinensis), and the closest known free-living relative (Laurencia obtusa) from the Canary Islands (Spain). For the first time we show parasitic red algal plastid genomes that are similar in size and gene content to free-living host species without any gene loss or genome reduction. The only exception was two pseudogenes (moeB and ycf46) found in the plastid genome of both isolates of J. tasmanica, indicating potential for future loss of these genes. Further comparative analyses with the three highly reduced plastid genomes showed possible gene loss patterns, in which photosynthetic gene categories were lost followed by other gene categories. Phylogenetic analyses did not confirm monophyly of Janczewskia, and the genus was subsumed into Laurencia. Further investigations will determine if any convergent small-scale patterns of gene loss exist in parasitic red algae and how these are applicable to other parasitic systems.

Reorganizing parasitic Delesseriaceae: taxonomic revision of Asterocolax

Red algal parasites are highly host specific organisms that are morphologically reduced with decreased pigmentation. Only found within the Florideophyceae, red algal parasites have evolved within eight orders, with the greatest parasite diversity found in the Ceramiales. A quarter of the ceramialian parasites in the family Delesseriaceae are described in the genus Asterocolax. The initial morphological description of Asterocolax led to the creation of an independent genus devoted to these parasitic species, but molecular data have repeatedly demonstrated that Asterocolax species, and likely many other red algal parasites, resolve within the genera of free-living red algae, often within the same genus as their hosts. Here and in previous studies, phylogenetic analysis of the internal transcribed spacer region of the ribosomal DNA has shown at least six instances of independent evolution of Asterocolax species, mainly interspersed among the free-living macroalgal genera of Phycodrys and Polyneura. As most Asterocolax are sister species to their hosts, they are independently derived from a photosynthetic ancestor, and together, do not form a monophyletic parasitic genus. Here we conduct a long overdue taxonomic revision of the red algal parasitic genus Asterocolax, describe a new species within the genus, and propose nomenclatural changes for four other species to reduce the polyphyletic clades encompassing Asterocolax.

Report of the 2021 meeting of the International Society of Protistologists.

THE International Society of Protistologists (ISOP) met online from 26-30 July, 2021. The Program and Abstract book for this is available here (File S1). An in-person international meeting was not possible due to the continued COVID-19 pandemic. The meeting therefore took place using the society's Zoom license, which is available for use by ISOP members for other online protist meetings.

The Organelle Genomes in the Photosynthetic Red Algal Parasite Pterocladiophila hemisphaerica (Florideophyceae, Rhodophyta) Have Elevated Substitution Rates and Extreme Gene Loss in the Plastid Genome.

Comparative organelle genome studies of parasites can highlight genetic changes that occur during the transition from a free-living to a parasitic state. Our study focuses on a poorly studied group of red algal parasites, which are often closely related to their red algal hosts and from which they presumably evolved. Most of these parasites are pigmented and some show photosynthetic capacity. Here, we assembled and annotated the complete organelle genomes of the photosynthetic red algal parasite, Pterocladiophila hemisphaerica. The plastid genome is the smallest known red algal plastid genome at 68,701bp. The plastid genome has many genes missing, including all photosynthesis-related genes. In contrast, the mitochondrial genome is similar in architecture to that of other free-living red algae. Both organelle genomes show elevated mutation rates and significant changes in patterns of selection, measured as dN/dS ratios. This caused phylogenetic analyses, even of multiple aligned proteins, to be unresolved or give contradictory relationships. Full plastid datasets interfered by selected best gene evolution models showed the supported relationship of P.hemisphaerica within the Ceramiales, but the parasite was grouped with support as sister to the Gracilariales when interfered under the GHOST model. Nuclear rDNA showed a supported grouping of the parasite within a clade containing several red algal orders including the Gelidiales. This photosynthetic parasite, which is unable to photosynthesize with its own plastid due to the total loss of all photosynthesis genes, raises intriguing questions on parasite-host organelle genome capabilities and interactions.

Response to Preuss and Zuccarello (2020): biological definitions that can be unambiguously applied for red algal parasites.

In response to a comment in this issue on our proposal of new terminology to distinguish red algal parasites, we clarify a few key issues. The terms adelphoparasite and alloparasite were previously used to identify parasites that infected close or distant relatives. However, most red algal parasites have only been studied morphologically, and molecular tools have shown that these binary terms do a poor job at representing the range of parasite-host relationships. We recognize the need to clarify inferred misconceptions that appear to be drawing from historical terminology to contaminate our new definitions. We did not intend to replace the term adelphoparasite with neoplastic parasites and the term alloparasites with archaeplastic parasites. Rather, we seek to establish new terms for discussing red algal parasites, based on the retention of a native plastid, a binary biological trait that is relatively easy to identify using modern methods and has biological implications for the interactions between a parasite and its host. The new terminology can better account for the spectrum of relationships and developmental patterns found among the many independently evolved red algal parasites, and it is intended to inspire new research, particularly the role of plastids in the survival and evolution of red algal parasites.

"Ectrogella" Parasitoids of the Diatom Licmophora sp. are Polyphyletic.

The diatom genera Licmophora and Fragilaria are frequent epiphytes on marine macroalgae and can be infected by intracellular parasitoids traditionally assigned to the oomycete genus Ectrogella. Much debate and uncertainty remains about the taxonomy of these oomycetes, not least due to their morphological and developmental plasticity. Here, we used single-cell techniques to obtain partial sequences of the parasitoids 18S and cox2 genes. The former falls into two recently identified clades of Pseudo-nitzschia parasites temporarily named OOM_1_2 and OOM_2, closely related to the genera of brown and red algal pathogens Anisolpidium and Olpidiopsis. A third group of sequences falls at the base of the red algal parasites assigned to Olpidiopsis. In one instance, two oomycete parasitoids seemed to co-exist in a single diatom cell; this co-occurrence of distinct parasitoid taxa not only within a population of diatom epiphytes, but also within the same host cell, possibly explains the ongoing confusion in the taxonomy of these parasitoids. We demonstrate the polyphyly of Licmophora parasitoids previously assigned to Ectrogella (sensu Sparrow, 1960) and show that parasites of red algae assigned to the genus Olpidiopsis are most likely not monophyletic. We conclude that combining single-cell microscopy and molecular methods is necessary for their full characterisation.

Molecular and morphological reappraisal of Spyridiocolax capixabus (Spyridiaceae, Rhodophyta), a rare endemic parasite from Brazil

Abstract The monotypic red algal parasite genus Spyridiocolax was proposed from material from the coast of Espírito Santo to accommodate Spyridiocolax capixabus, endemic from Brazil. The species is rare, and we performed a morphological reappraisal and the first molecular characterization of S. capixabus. Parasite specimens growing on Spyridia clavata were collected in the type locality, Itaoca Beach, Espírito Santo. Spyridiocolax capixabus forms colorless warts on the branches of S. clavata, and the secondary pit connections were described for the first time. Male, female and tetrasporophytic structures were observed growing in the same host plant. The plastid rbcL sequences of parasite and host were identical. A divergence of one nucleotide was found to the nuclear SSU rRNA gene, suggesting that the parasite retains the chloroplast of its host. Both plastidial and nuclear phylogenies supported the close relationship of S. capixabus and S. clavata. The data obtained corroborate other studies with rhodophycean parasites, which show morphological and molecular similarities between parasites and hosts. To maintain the monophyly of the host genus, the transfer of S. capixabus to Spyridia is proposed here on the basis of morphological and molecular evidence. Our study constitutes a starting point for reinvestigating the red algal parasites in Brazil.

Development of the red algal parasite Vertebrata aterrimophila sp. nov. (Rhodomelaceae, Ceramiales) from New Zealand

ABSTRACTParasitic red algae grow only on other red algae and have over 120 described species. Developmental studies in red algal parasites are few, although they have shown that secondary pit connections formed between parasite and host and proposed that this was an important process in successful parasitism. Furthermore, it was recorded that the transfer of parasite nuclei by these secondary pit connections led to different host cell effects. We used developmental studies to reconstruct early stages and any host cell effects of a parasite on Vertebrata aterrima. A mitochondrial marker (cox1) and morphological observations (light and fluorescence microscopy) were used to describe this new red algal parasite as Vertebrata aterrimophila sp. nov. Early developmental stages show that a parasite spore connects via secondary pit connections with a pericentral host cell after cuticle penetration. Developmental observations revealed a unique connection cell that grows into a ‘trunk-like’ structure. Host cell transformation after infection by the parasite included apparent increases in both carbohydrate concentrations and nuclear size, as well as structural changes. Analyses of molecular phylogenies and reproductive structures indicated that the closest relative of V. aterrimophila is its host, V. aterrima. Our study shows a novel developmental parasite stage (‘trunk-like’ cell) and highlights the need for further developmental studies to investigate the range of developmental patterns and host effects in parasitic red algae.

Molecular phylogenetics supports a clade of red algal parasites retaining native plastids: taxonomy and terminology revised.

Parasitism is a life strategy that has repeatedly evolved within the Florideophyceae. Historically, the terms adelphoparasite and alloparasite have been used to distinguish parasites based on the relative phylogenetic relationship of host and parasite. However, analyses using molecular phylogenetics indicate that nearly all red algal parasites infect within their taxonomic family, and a range of relationships exist between host and parasite. To date, all investigated adelphoparasites have lost their plastid, and instead, incorporate a host-derived plastid when packaging spores. In contrast, a highly reduced plastid lacking photosynthesis genes was sequenced from the alloparasite Choreocolax polysiphoniae. Here we present the complete Harveyella mirabilis plastid genome, which has also lost genes involved in photosynthesis, and a partial plastid genome from Leachiella pacifica. The H.mirabilis plastid shares more synteny with free-living red algal plastids than that of C.polysiphoniae. Phylogenetic analysis demonstrates that C.polysiphoniae, H.mirabilis, and L.pacifica form a robustly supported clade of parasites, which retain their own plastid genomes, within the Rhodomelaceae. We therefore transfer all three genera from the exclusively parasitic family, Choreocolacaceae, to the Rhodomelaceae. Additionally, we recommend applying the terms archaeplastic parasites (formerly alloparasites), and neoplastic parasites (formerly adelphoparasites) to distinguish red algal parasites using a biological framework rather than taxonomic affiliation with their hosts.

Holocarpic oomycete parasitoids of red algae are not Olpidiopsis.

Olpidiopsis is a genus of obligate holocarpic endobiotic oomycetes. Most of the species classified in the genus are known only from their morphology and life cycle, and a few have been examined for their ultrastructure or molecular phylogeny. However, the taxonomic placement of all sequenced species is provisional, as no sequence data are available for the type species, O. saprolegniae, to consolidate the taxonomy of species currently placed in the genus. Thus, efforts were undertaken to isolate O. saprolegniae from its type host, Saprolegnia parasitica and to infer its phylogenetic placement based on 18S rDNA sequences. As most species of Olpidiopsis for which sequence data are available are from rhodophyte hosts, we have also isolated the type species of the rhodophyte-parasitic genus Pontisma, P. lagenidioides and obtained partial 18S rDNA sequences. Phylogenetic reconstructions in the current study revealed that O. saprolegniae from Saprolegnia parasitica forms a monophyletic group with a morphologically similar isolate from S. ferax, and a morphologically and phylogenetically more divergent species from S. terrestris. However, they were widely separated from a monophyletic, yet unsupported clade containing P. lagenidioides and red algal parasites previously classified in Olpidiopsis. Consequently, all holocarpic parasites in red algae should be considered to be members of the genus Pontisma as previously suggested by some researchers. In addition, a new species of Olpidiopsis, O. parthenogenetica is introduced to accommodate the pathogen of S. terrestris.

Comparative studies of photosynthetic capacity in three pigmented red algal parasites: Chlorophyll a concentrations and PAM fluorometry measurements

SUMMARYOver 100 species of red algae have been described as parasites on other red algae, but the majority show some degree of pigmentation. This raises the question of their parasitic status, especially their abilities to photosynthesize and their dependence on their host for fixed carbon. Are they considered parasites only based on morphological characters, for example, reduced size and secondary pit connection to the host? Translocation of nutrients from host to parasite have been shown for very few red algal parasites, and these were mostly unpigmented. This study investigated three pigmented red algal parasites (Rhodophyllis parasitica, Vertebrata aterrimophila and Pterocladiophila hemisphaerica) from New Zealand. We quantified their chlorophyll a content and also measured their PSII capacity using PAM fluorometry. All three parasites contained chlorophyll a. The parasites Rhodophyllis parasitica and Vertebrata aterrimophila were not able to photosynthesize and must therefore be fully nutritional dependent on their host. The parasite Pterocladiophila hemisphaerica was able to photosynthesize independently, but based on molecular characteristics we suggest that it relies on the host plastid to do photosynthesis. Our results support the parasitic status of all three species and highlights the necessity of more studies investigating the differences in host dependency in red algal parasites.

Three new red algal parasites from New Zealand: Cladhymenia oblongifoliaphila sp. nov. (Rhodomelaceae), Phycodrys novae-zelandiaephila sp. nov. (Delesseriaceae) and Judithia parasitica sp. nov. (Kallymeniaceae)

:There are over 120 species of red algal parasites (Florideophyceae) but they are often overlooked due to their small size and patchy distribution. Red algal parasites have mostly been described as independent genera but recent phylogenetic studies have shown that parasites are related to free-living relatives, often their hosts, and have been named in these genera to maintain monophyly. We investigated the morphology, distribution and phylogeny, using diverse molecular markers (mitochondrial, nuclear, plastid), of three new red algal parasites in New Zealand. We describe the parasites using morphological and anatomical observations and estimate their distribution by surveying herbarium vouchers. Analyses of reproductive structures and molecular phylogenies indicate that the closest relative of the parasite Phycodrys novae-zelandiaephila sp. nov. is its host, Phycodrys novae-zelandiae. Based on nuclear and mitochondrial markers, the closest relative of the parasite Cladhymenia oblongifoliaphila sp. nov. is its host Cladhymenia oblongifolia but plastid markers group it with Cladhymenia lyallii, suggesting that this species was a past host and the source of parasite plastids. The parasite Judithia parasitica sp. nov. groups with Judithia delicatissima but infects Blastophyllis spp., suggesting that this parasite evolved as a free-living or parasitic Judithia species, and host switching may have occurred. This study adds to our knowledge of New Zealand red algal parasites and highlights contrasting patterns of host–parasite relationships.

Parasitism finds many solutions to the same problems in red algae (Florideophyceae, Rhodophyta)

Parasitic red algae evolve from a common ancestor with their hosts, parasitizing cousins using familiar cellular mechanisms. They have independently evolved over one hundred times within the exclusively multicellular red algal class Florideophyceae. Reduced morphology, a lack of pigmentation, and direct cell–cell connections with their hosts are markers of red algal parasitism. With so many potential evolutionary pathways, red algal parasite diversity offers a unique test case to understand the earliest stages of this lifestyle transition. Molecular and morphological investigations led to the categorization of these parasites based on their relationship to their host. “Adelphoparasites” are phylogenetically close to their hosts, often infecting a sister species, whereas “alloparasites” are more distantly related to their hosts. The differentiation of these parasites, based on their phylogenetic relationship to their host, has resulted in a simplified classification of these parasites that may not reflect the many evolutionary pathways they take to arrive at a similar endpoint. Accordingly, many parasites fall into a gray area between adelphoparasite and alloparasite definitions, challenging the established features we use to classify them. Molecular phylogenetic research has been essential in identifying gaps in knowledge, but microscopy needs to be reincorporated in order to address red algal parasite developmental variation to establish a new paradigm. The joint utilization of molecular and microscopic methods will be critical in identifying the genomic and physiological traits of both nascent and well-established parasites.

Red algal parasites: a synopsis of described species, their hosts, distinguishing characters and areas for continued research

Abstract Red algal parasites are diverse organisms that are unusual due to the fact that many are closely related to their hosts. Parasitism has developed many times within different red algal groups, but the full extent of parasite biodiversity is unknown, as parasites are easily overlooked due to their small size and often low abundance. Additionally, the literature on red algal parasites is dispersed and has not been compiled in over 30 years. Although criteria have been proposed to define what constitutes a red algal parasite, many parasites are poorly described, and the cellular interactions with their host are poorly known. A few studies have demonstrated that parasites transfer organelles to host cells, which can alter the physiology of the host to the benefit of the parasite. Here, we apply a set of defining criteria for parasites to a compiled list of all described red algal parasites. Our results highlight the lack of knowledge of many key parasitic processes including early parasite development, host cell “control”, and parasite origin. Until the biology of more parasites is studied, generalisations on the processes of parasitism in red algae may be premature. We hope this synopsis will stimulate research into this fascinating group.

Red Algal Mitochondrial Genomes Are More Complete than Previously Reported.

The enslavement of an alpha-proteobacterial endosymbiont by the last common eukaryotic ancestor resulted in large-scale gene transfer of endosymbiont genes to the host nucleus as the endosymbiont transitioned into the mitochondrion. Mitochondrial genomes have experienced widespread gene loss and genome reduction within eukaryotes and DNA sequencing has revealed that most of these gene losses occurred early in eukaryotic lineage diversification. On a broad scale, more recent modifications to organelle genomes appear to be conserved and phylogenetically informative. The first red algal mitochondrial genome was sequenced more than 20 years ago, and an additional 29 Florideophyceae mitochondria have been added over the past decade. A total of 32 genes have been described to have been missing or considered non-functional pseudogenes from these Florideophyceae mitochondria. These losses have been attributed to endosymbiotic gene transfer or the evolution of a parasitic life strategy. Here we sequenced the mitochondrial genomes from the red algal parasite Choreocolax polysiphoniae and its host Vertebrata lanosa and found them to be complete and conserved in structure with other Florideophyceae mitochondria. This result led us to resequence the previously published parasite Gracilariophila oryzoides and its host Gracilariopsis andersonii, as well as reevaluate reported gene losses from published Florideophyceae mitochondria. Multiple independent losses of rpl20 and a single loss of rps11 can be verified. However by reannotating published data and resequencing specimens when possible, we were able to identify the majority of genes that have been reported as lost or pseudogenes from Florideophyceae mitochondria.

Small-scale genetic structure of Gracilaria salicornia and its red algal parasite, G. babae (Gracilariaceae, Rhodophyta), in Malaysia

Abstract The present study compares genetic structure from the plastid rbcL, mitochondrial cox1, and nuclear internal transcribed spacer (ITS) sequences among 13 populations of Gracilaria salicornia and its red algal parasite, G. babae, in Malaysia. Owing to the unique biology of the red algal parasite, identical phylogeographies were inferred from the rbcL and cox1 sequences in both G. babae and its host, G. salicornia. Despite the low genetic variation, rbcL and cox1 showed a concordant phylogeographic split that largely corresponds to Peninsular Malaysia and East Malaysia, except for a sample from East Malaysia that was consistently grouped with samples from the peninsula. On the other hand, G. salicornia was separated from G. babae in the midpoint-rooted phylogeny inferred from ITS data despite the failure to retrieve the two taxa in reciprocal monophyly. Gracilaria salicornia was less diverse and lacked apparent geographic structure. In contrast, the ITS data revealed considerable genetic diversity and fine-scale genetic structuring in G. babae within Malaysian waters, probably as a result of adaptation to the local host population.

What's in a name? Monophyly of genera in the red algae: Rhodophyllis parasitica sp. nov. (Gigartinales, Rhodophyta); a new red algal parasite from New Zealand

Red algal parasites are common within red algae and are mostly closely related to their hosts, but have a reduced habit. In the past, red algal parasites, due to their reduced morphology, have been given distinct generic names, even though they are often phylogenetically nested in their host’s genus. This is a problem nomenclaturally for maintenance of a taxonomy based on monophyly. This study investigates the morphology, genetic variation and distribution of an unde-scribed red algal parasite growing on its host

Are all red algal parasites cut from the same cloth?

Parasitism is a common life strategy throughout the eukaryotic tree of life. Many devastating human pathogens, including the causative agents of malaria and toxoplasmosis, have evolved from a photosynthetic ancestor. However, how an organism transitions from a photosynthetic to a parasitic life history strategy remains mostly unknown. This is largely because few systems present the opportunity to make meaningful comparisons between a parasite and a close free-living relative. Parasites have independently evolved dozens of times throughout the Florideophyceae (Rhodophyta), and often infect close relatives. The accepted evolutionary paradigm proposes that red algal parasites arise by first infecting a close relative and over time diversify and infect more distantly related species. This provides a natural evolutionary gradient of relationships between hosts and parasites that share a photosynthetic common ancestor. Elegant microscopic work in the late 20th century provided detailed insight into the infection cycle of red algal parasites and the cellular interactions between parasites and their hosts. Those studies led to the use of molecular work to further investigate the origins of the parasite organelles and reveal the evolutionary relationships between hosts and their parasites. Here we synthesize the research detailing the infection methods and cellular interactions between red algal parasites and their hosts. We offer an alternative hypothesis to the current dogma of red algal parasite evolution and propose that red algae can adopt a parasitic life strategy through multiple evolutionary pathways, including direct infection of distant relatives. Furthermore, we highlight potential directions for future research to further evaluate parasite evolution in red algae.

Red algal parasites: Models for a life history evolution that leaves photosynthesis behind again and again

Many of the most virulent and problematic eukaryotic pathogens have evolved from photosynthetic ancestors, such as apicomplexans, which are responsible for a wide range of diseases including malaria and toxoplasmosis. The primary barrier to understanding the early stages of evolution of these parasites has been the difficulty in finding parasites with closely related free-living lineages with which to make comparisons. Parasites found throughout the florideophyte red algal lineage, however, provide a unique and powerful model to investigate the genetic origins of a parasitic lifestyle. This is because they share a recent common ancestor with an extant free-living red algal species and parasitism has independently arisen over 100 times within this group. Here, we synthesize the relevant hypotheses with respect to how these parasites have proliferated. We also place red algal research in the context of recent developments in understanding the genome evolution of other eukaryotic photosynthesizers turned parasites.

A new red algal parasite, Symphyocolax koreana gen. et sp. nov. (Rhodomelaceae, Ceramiales), from Korea

A new red algal parasite, Symphyocolax koreana M. S. Kim, gen. et sp. nov., has been found on a specimen of Symphyocladia latiuscula (Harvey) Yamada, a member of the tribe Pterosiphonieae of the Rhodomelaceae; this genus has never before been reported to host red algal parasites. Here, the new parasite from Korea is described in terms of vegetative and reproductive morphology. The thallus has a minute, colored polysiphonous upright axis with many branches attached by pseudoparenchymatous pulvinate bases. There are six pericentral cells, with many corticated cells in the lower part of the main branches. Trichoblasts occur on dioecious male and female gametophytes, but not on tetrasporophytes. Procarps develop on suprabasal cells of trichoblasts and consist of a four-celled carpogonial branch and two sterile cells attached to the supporting cell. Spermatangial branches are borne one per each successive segment on monosiphonous pedicels in spiral positions with fertile trichoblast. Tetrasporangia are formed one per segment in a straight series and are tetrahedrally divided. Features of the vegetative axes, procarp, spermatangial trichoblasts, and tetrasporangial branching show that the new genus is an alloparasite belonging to the tribe Polysiphonieae.