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

Gregarine single-cell transcriptomics reveals differential mitochondrial remodeling and adaptation in apicomplexans

BackgroundApicomplexa is a diverse phylum comprising unicellular endobiotic animal parasites and contains some of the most well-studied microbial eukaryotes including the devastating human pathogens Plasmodium falciparum and Cryptosporidium hominis. In contrast, data on the invertebrate-infecting gregarines remains sparse and their evolutionary relationship to other apicomplexans remains obscure. Most apicomplexans retain a highly modified plastid, while their mitochondria remain metabolically conserved. Cryptosporidium spp. inhabit an anaerobic host-gut environment and represent the known exception, having completely lost their plastid while retaining an extremely reduced mitochondrion that has lost its genome. Recent advances in single-cell sequencing have enabled the first broad genome-scale explorations of gregarines, providing evidence of differential plastid retention throughout the group. However, little is known about the retention and metabolic capacity of gregarine mitochondria.ResultsHere, we sequenced transcriptomes from five species of gregarines isolated from cockroaches. We combined these data with those from other apicomplexans, performed detailed phylogenomic analyses, and characterized their mitochondrial metabolism. Our results support the placement of Cryptosporidium as the earliest diverging lineage of apicomplexans, which impacts our interpretation of evolutionary events within the phylum. By mapping in silico predictions of core mitochondrial pathways onto our phylogeny, we identified convergently reduced mitochondria. These data show that the electron transport chain has been independently lost three times across the phylum, twice within gregarines.ConclusionsApicomplexan lineages show variable functional restructuring of mitochondrial metabolism that appears to have been driven by adaptations to parasitism and anaerobiosis. Our findings indicate that apicomplexans are rife with convergent adaptations, with shared features including morphology, energy metabolism, and intracellularity

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

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

The ghost plastid of Choreocolax polysiphoniae

Parasitism has evolved innumerable times among eukaryotes. Red algal parasites alone have independently evolved over 100 times. The accepted evolutionary paradigm proposes that red algal parasites arise by first infecting a close relative and over time diversifying and infecting more distantly related species. This provides a natural evolutionary gradient of relationships between hosts and parasites that share a photosynthetic common ancestor. Upon infection, the parasite deposits its organelles into the host cell and takes over, spreading through cell-cell connections. Microscopy and molecular studies have demonstrated that the parasites do not maintain their own plastid, but rather abscond with a dedifferentiated host plastid as they pack up spores for dispersal. We sequenced a ~90 kb plastid genome from the parasite Choreocolax polysiphoniae, which has lost genes for light harvesting and photosynthesis. Furthermore, the presence of a native C. polysiphoniae plastid indicates that not all red algal parasites follow the same evolutionary pathway to parasitism. Along with the 167 kb plastid genome of its host, Vertebrata lanosa, these plastids are the first to be sequenced from the Ceramiales

Kelp transcriptomes provide robust support for interfamilial relationships and revision of the little known Arthrothamnaceae (Laminariales)

If ever there were “charismatic megaflora” of the sea, the Laminariales (kelp) would undoubtedly meet that designation. From the Northeast Pacific kelp forests to the less diverse, but nonetheless dense, kelp beds ranging from the Arctic to the cold temperate waters of the Southern Hemisphere, kelp provide habitat structure and food for a variety of productive marine systems. Consequently, kelp are well represented in the literature, however, understanding their evolution has proven challenging. We used a 152-gene phylogenomics approach to better resolve the phylogeny of the “derived” kelp families (viz., Agaraceae, Alariaceae, Laminariaceae, and Lessoniaceae). The formerly unresolved Egregia menziesii firmly joined a significantly expanded Arthrothamnaceae including Arthrothamnus, Cymathaere, Ecklonia, Macrocystis, Nereocystis, Pelagophycus, Postelsia, Pseudolessonia, Saccharina, and Streptophyllopsis, which rendered both the Laminariaceae and Lessoniaceae monogeneric. A published eight-gene alignment, the most marker-rich prior to this study, was expanded and analyzed to facilitate inclusion of Aureophycus. Although the topology was unchanged at the family level between the transcriptome data set relative to eight-gene analyses, the superior resolving power of the former was clearly established

A contaminant DNA barcode sequence reveals a newred algal order, Corynodactylales (Nemaliophycidae, Florideophyceae)

Routine DNA barcode surveys of red algae can occasionally yield contaminant sequences owing to the diverse epi/endo flora and fauna that can inhabit these species. Often discarded as nuisance data, further exploration in this study led to the discovery of an unusual red alga with a highly characteristic vegetative development in which the diminutive primary vegetative filaments are terminated by distinctive monosporangia. This entity is described here as Corynodactylus rejiciendus G.W. Saunders gen. et sp. nov. Generating genomic data from the host and associated epiphytic flora, and subsequently subtracting out genes of the former, facilitated a multigene phylogenetic analysis supporting recognition of Corynodactylaceae fam. nov. and Corynodactylales ord. nov. as a distant sister to the order Balliales in the subclass Nemaliophycidae

Global sampling reveals low genetic diversity within Compsopogon (Compsopogonales, Rhodophyta)

Twenty-five specimens of the freshwater red alga Compsopogon were collected from locations in North America, South America, Europe, Asia, Australasia and Oceania, and from an aquarium, with the goal of determining genetic diversity among specimens and ascertaining the number of phylogenetic species. Specimens were morphologically identified as having either the 'caeruleus' morphology, with regular polyhedral cortical cells, or the 'leptoclados' morphology, with irregular cortical cells with rhizoidal outgrowths. The 'leptoclados' morphology has been used by some researchers to distinguish the genus Compsopogonopsis from Compsopogon, or at least to distinguish C. leptoclados from other Compsopogon species. Sequence data for the rbcL gene and cox1 barcoding region were obtained for most specimens. In addition, SSU and partial LSU (barcode) rDNA were explored for a few specimens, but all sequences were identical. For the 25 newly generated and eight previously published rbcL gene data, there were seven unique haplotypes, but the sequence divergence was very low (≤7 bp, ≤ 0.7%). One haplotype was widespread, represented by 21 specimens from diverse locations in all regions sampled. Likewise, the 22 new and one previously published cox1 barcode region sequences yielded seven unique haplotypes with little sequence divergence (≤13 bp, ≤ 2.0%). One haplotype was widespread, being shared among 16 specimens from all regions. The combined molecular and morphological data showed no genetic differentiation between the 'caeruleus' and 'leptoclados' morphologies. The ubiquitous distribution of Compsopogon in tropical/subtropical regions and its low genetic variation are probably facilitated by the alga's ability to tolerate a wide range of stream conditions and its propagation via asexual spores. Given the findings of previous culture-based studies, morphometric research and field observations, coupled with the results of our study, we conclude there is only a single monospecific genus worldwide and that the species is correctly called C. caeruleus, since this is the oldest validly published name; all other previously described species of Compsopogon and Compsopogonopsis are synonyms. © 2013 British Phycological Society