Adrian Reyes-Prieto

• Associate Professor
• Professor (Associate) at University of New Brunswick

The loss of photosynthesis is frequently associated with parasitic or pathogenic lifestyles, but it can also occur in free-living, plastid-bearing lineages. A common consequence of becoming non-photosynthetic is the reduction in size and gene content of the plastid genome. In exceptional circumstances, it can even result in the complete loss of the...

The endosymbiotic origin of plastids was a launching point for eukaryotic evolution. The autotrophic abilities bestowed by plastids are responsible for much of the eukaryotic diversity we observe today. But despite its many advantages, photosynthesis has been lost numerous times and in disparate lineages throughout eukaryote evolution. For example,...

The Glaucophyta is one of the three major lineages of photosynthetic eukaryotes, together with viridiplants and red algae, united in the presumed monophyletic supergroup Archaeplastida. Glaucophytes constitute a key algal lineage to investigate both the origin of primary plastids and the evolution of algae and plants. Glaucophyte plastids possess e...

A significant limitation when testing the putative single origin of primary plastids and the monophyly of the Archaeplastida supergroup, comprised of the red algae, viridiplants, and glaucophytes, is the scarce nuclear and organellar genome data available from the latter lineage. The Glaucophyta are a key algal group when investigating the origin a...

Some mat‐forming cyanobacteria produce harmful cyanotoxins, yet benthic species remain understudied compared to planktonic counterparts. This study assesses the diversity, distribution and toxin production of mat‐forming cyanobacteria across lentic and lotic systems in Nova Scotia, Canada. We documented greater cyanobacterial species richness in le...

The marine archaeon Methanosarcina acetivorans contains a putative NAD + -independent d-lactate dehydrogenase (D-iLDH/glycolate oxidase) encoded by the MA4631 gene, belonging to the FAD-oxidase C superfamily. Nucleotide sequences similar to MA4631 gene, were identified in other methanogens and Firmicutes with >90 and 35-40% identity, respectively....

Protists (microbial eukaryotes) are a critically important but understudied group of microorganisms. They are ubiquitous, represent most of the genetic and functional diversity among eukaryotes, and play essential roles in nutrient and energy cycling. Yet, protists remain a black box in marine sedimentary ecosystems like the intertidal mudflats in...

The presence of toxigenic benthic cyanobacteria in riverine ecosystems is an increasing concern around the world. In 2018, the death of three dogs along the Wolastoq (also known as the Saint John River) in New Brunswick, Canada, was attributed to anatoxin exposure after they ingested benthic microbial mats found along the shore. Here, we shotgun se...

The loss of photosynthesis in land plants and algae is typically associated with parasitism but can also occur in free‐living species, including chlamydomonadalean green algae. The plastid genomes (ptDNAs) of colorless chlamydomonadaleans are surprisingly diverse in architecture, including highly expanded forms (Polytoma uvella and Leontynka pallid...

Genes of unknown function constitute a considerable fraction of most bacterial genomes. In a Tn5-based search for stress response genes in the nitrogen-fixing facultative endosymbiont Sinorhizobium (Ensifer) meliloti, we identified a previously uncharacterized gene required for growth on solid media with increased NaCl concentrations. The encoded p...

Understanding how cooperation evolved and is maintained remains an important and often controversial topic because cheaters that reap the benefits of cooperation without paying the costs can threaten the evolutionary stability of cooperative traits. Cooperation—and especially reproductive altruism—is particularly relevant to the evolution of multic...

The loss of photosynthesis in land plants and algae is typically associated with parasitism but can also occur in free-living species, including chlamydomonadalean green algae. The plastid genomes (ptDNAs) of colorless chlamydomonadalean species are surprisingly diverse in architecture, including highly expanded forms ( Polytoma uvella, Leontynka p...

Cyanobacterial blooms and their toxigenic potential threaten freshwater resources worldwide. In Atlantic Canada, despite an increase of cyanobacterial blooms in the last decade, little is known about the toxigenic potential and the taxonomic affiliation of bloom-forming cyanobacteria. In this study, we employed polymerase chain reaction (PCR) and m...

Glaucophytes, red algae and viridiplants (green algae and land plants) are formally united in the supergroup Archaeplastida. Although diverse molecular and genomic evidence suggest the common origin of the three Archaeplastida lineages, the lack of a robust glaucophyte knowledgebase has limited comprehensive evaluations of competing hypotheses. Gla...

Cyanotoxins are an emerging threat to freshwater resources worldwide. The most frequently reported cyanotoxins are the microcystins, which threaten the health of humans, wildlife, and ecosystems. Determining the potential for microcystin production is hindered by a lack of morphological features that correlate with microcystin production. However,...

Winogradsky columns have been widely used to study soil microbial communities, but the vast majority of those investigations have focused on the ecology and diversity of bacteria. In contrast, microbial eukaryotes (ME) have been regularly overlooked in studies based on experimental soil columns. Despite the recognized ecological relevance of ME in...

Cyanophora is the glaucophyte model taxon. Following the sequencing of the nuclear genome of C. paradoxa, studies based on single organelle and nuclear molecular markers revealed previously unrecognized species diversity within this glaucophyte genus. Here, we present the complete plastid (ptDNA) and mitochondrial (mtDNA) genomes of C. kugrensii, C...

Plastid genome (ptDNA) data of Glaucophyta have been limited for many years to the genus Cyanophora. Here, we sequenced the ptDNAs of Gloeochaete wittrockiana, Cyanoptyche gloeocystis, Glaucocystis incrassata, and Glaucocystis sp. BBH. The reported sequences are the first genome-scale plastid data available for these three poorly studied glaucophyt...

The chloroplast genomes (cpDNA) of five Chlamydomonas reinhardtii nonphotosynthetic mutants were sequenced. The architecture, gene content, and synteny of the cpDNAs from the five mutants are identical to the C. reinhardtii ‘wild-type’ plastome. A small number of differences at sequence level between coding regions of the reference genome and the c...

The thing about plastid genomes in nonphotosynthetic plants and algae is that they are usually very small and highly compact. This is not surprising: a heterotrophic existence means that genes for photosynthesis can be easily discarded. But the loss of photosynthesis cannot explain why the plastomes of heterotrophs are so often depauperate in nonco...

Diverse studies of plastid data suggest that the photosynthetic organelles of red algae, viridiplants, and glaucophytes, the three lineages comprising the Archaeplastida supergroup, share a common ancestor. Glaucophyte plastids are unique among archaeplastidians due to the presence of a vestigial peptidoglycan wall and the accumulation of RuBisCO i...

Mitochondria arose from bacterial endosymbionts. One of the consequences of the endosymbiosis event was that the ancestral bacterial genome underwent deep transformations, including massive gene transfer to the host nucleus and gene losses and rearrangements. Upon eukaryotic origin, the gene content, size and shape of mitochondrial genomes evolved...

The origin of photosynthetic organelles via endosymbiosis more than 1 Gya ago was a major detonator of eukaryotic diversification. The evolution of a stable endosymbiotic relationship between eukaryotic cells and photosynthetic cyanobacteria involved series of cellular and molecular processes that are not entirely understood. Critical steps toward...

The mitochondrial genomes of chlamydomonadalean green algae are renowned for their highly reduced and conserved gene repertoires, which are almost fixed at 12 genes across the entire lineage. The sizes of these genomes, however, are much more variable, with some species having small, compact mitochondrial DNAs (mtDNAs) and others having expanded on...

Vitamin B1 (thiamine pyrophosphate, TPP) is essential to all life but scarce in ocean surface waters. In many bacteria and a few eukaryotic groups thiamine biosynthesis genes are controlled by metabolite-sensing mRNA-based gene regulators known as riboswitches. Using available genome sequences and transcriptomes generated from ecologically importan...

Significance Phytochromes are photosensory signaling proteins widely distributed in unicellular organisms and multicellular land plants. Best known for their global regulatory roles in photomorphogenesis, plant phytochromes are often assumed to have arisen via gene transfer from the cyanobacterial endosymbiont that gave rise to photosynthetic chlor...

The sodium -pumping NADH: ubiquinone oxidoreductase (Na+-NQR) is the main ion pump and the primary entry site for electrons into the respiratory chain of many different types of pathogenic bacteria. This enzymatic complex creates a transmembrane gradient of sodium that is used by the cell to sustain ionic homeostasis, nutrient transport, ATP synthe...

The phytochelatin synthase from photosynthetic Euglena gracilis (EgPCS) was analyzed at the transcriptional, kinetic, functional, and phylogenetic levels. Recombinant EgPCS was a monomeric enzyme able to synthesize, in the presence of Zn(2+) or Cd(2+), phytochelatin2-phytochelatin4 (PC2-PC4) using GSH or S-methyl-GS (S-methyl-glutathione), but not...

Photosynthetic eukaryotes comprise the most visible and massive fraction of the biosphere. They have contributed to shaping land, oceans, and atmosphere during the last 2 billion years and their influence dominates every aspect of the existence of the rest of living beings, humans included. The introduction of photosynthesis into the eukaryotic dom...

Photosynthetic eukaryotes comprise the most visible and massive fraction of the biosphere. They have contributed to shaping land, oceans, and atmosphere during the last 2 billion years and their influence dominates every aspect of the existence of the rest of living beings, humans included. The introduction of photosynthesis into the eukaryotic dom...

Studies of photosynthetic eukaryotes have revealed that the evolution of plastids from cyanobacteria involved the recruitment of non-cyanobacterial proteins. Our phylogenetic survey of >100 Arabidopsis nuclear-encoded plastid enzymes involved in amino acid biosynthesis identified only 21 unambiguous cyanobacterial-derived proteins. Some of the seve...

Supplementary Information

Cryptophyte and chlorarachniophyte algae are transitional forms in the widespread secondary endosymbiotic acquisition of photosynthesis by engulfment of eukaryotic algae. Unlike most secondary plastid-bearing algae, miniaturized versions of the endosymbiont nuclei (nucleomorphs) persist in cryptophytes and chlorarachniophytes. To determine why, and...

The evolution of microbial eukaryotes, in particular of photosynthetic lineages, is complicated by multiple instances of endosymbiotic and horizontal gene transfer (E/HGT) resulting from plastid origin(s). Our recent analysis of diatom membrane transporters provides evidence of red and/or green algal origins of 172 of the genes encoding these prote...

Plastid Origins The glaucophytes, represented by the alga Cyanophora paradoxa , are the putative sister group of red and green algae and plants, which together comprise the founding group of photosynthetic eukaryotes, the Plantae. In their analysis of the genome of C. paradoxa , Price et al. (p. 843 ; see the Perspective by Spiegel ) demonstrate a...

Alga is an informal name that refers to a diverse group of photosynthetic eukaryotes that have a polyphyletic origin in the tree of life. Although genomics has provided powerful tools for understanding the evolution of algal photosynthesis many issues remain unresolved. These include explaining the intermingling of plastid-lacking taxa such as cili...

The primary endosymbiotic origin of the plastid in eukaryotes more than 1 billion years ago led to the evolution of algae and plants. We analyzed draft genome and transcriptome data from the basally diverging alga Cyanophora paradoxa and provide evidence for a single origin of the primary plastid in the eukaryote supergroup Plantae. C. paradoxa ret...

The number of protein sequences in the database that is used for the phylogenomic analysis in this study, based on phyla. (DOCX)

Distribution of phyla with exclusive BLASTP hits to diatom MT proteins across the minimum number of hits per query, x ≥2, ≥10, and ≥20. (PDF)

Manual inspection of the 399 phylogenetically meaningful trees after initial computational screening. See also Dataset S1. (XLSX)

The list of 55 genes of Chlamydiae-like origin that were found in the 17 Plantae genomes analyzed in this study using phylogenomic methods. Shown are the tree IDs, the source of the sequences, the GI/accession numbers in the source database, the gene annotations in that database, the Arabidopsis homolog GI numbers and putative functions, the Chlamy...

Summary of 1,014 diatom MTs used in this study based on their putative function, gene origin and protein target. (XLSX)

All 1,014 protein sequences of diatom MTs used in this study. (TXT)

Analysis of algal E/HGT in stramenopiles across 75 diatom MTs based on topological comparison against a null hypothesis. (XLSX)

Membrane transporters (MTs) facilitate the movement of molecules between cellular compartments. The evolutionary history of these key components of eukaryote genomes remains unclear. Many photosynthetic microbial eukaryotes (e.g., diatoms, haptophytes, and dinoflagellates) appear to have undergone serial endosymbiosis and thereby recruited foreign...

The cyanobacterium-derived plastids of algae and plants have supported the diversification of much of extant eukaryotic life. Inferences about early events in plastid evolution must rely on reconstructing events that occurred over a billion years ago. In contrast, the photosynthetic amoeba Paulinella chromatophora provides an exceptional model to s...

Algae are a heterogeneous group of protists with multiple phylogenetic origins (i.e., they are polyphyletic) that include all photosynthetic eukaryotes except land plants. Despite being a nonnatural assemblage, the term alga as referring to aquatic primary producers is valuable in an ecological context and has wide usage in biology. Recent genomic...

The Chromalveolata "supergroup" is a massive assemblage of single-celled and multicellular protists such as ciliates and kelps that remains to be substantiated in molecular trees. Recent multigene analyses place chromalveolates into two major clades, the SAR (Stramenopiles, Alveolata, and Rhizaria) and the Cryptophyta+Haptophyta. Here we determined...

Gaining the ability to photosynthesize was a key event in eukaryotic evolution because algae and plants form the base of the food chain on our planet. The eukaryotic machines of photosynthesis are plastids (e.g., chloroplast in plants) that evolved from cyanobacteria through primary endosymbiosis. Our knowledge of plastid evolution, however, remain...

Plantae (as defined by Cavalier-Smith, 1981) [1 • Cavalier-Smith T. Eukaryote kingdoms: seven or nine?.Biosystems. 1981; 14: 461-481 • Crossref • PubMed • Scopus (270) • Google Scholar ] plastids evolved via primary endosymbiosis whereby a heterotrophic protist enslaved a photosynthetic cyanobacterium. This “primary” plastid spread into other euk...

Two genes encoding cytochrome c oxidase subunits, Cox2a and Cox2b, are present in the nuclear genomes of apicomplexan parasites and show sequence similarity to corresponding genes in chlorophycean algae. We explored the presence of COX2A and COX2B subunits in the cytochrome c oxidase of Toxoplasma gondii. Antibodies were raised against a synthetic...

The photosynthetic organelle (plastid) originated via primary endosymbiosis in which a phagotrophic protist captured and harnessed a cyanobacterium. The plastid was inherited by the common ancestor of the red, green (including land plants), and glaucophyte algae (together, the Plantae). Despite the critical importance of primary plastid endosymbios...

What factors drove the transformation of the cyanobacterial progenitor of plastids (e.g. chloroplasts) from endosymbiont to bona fide organelle? This question lies at the heart of organelle genesis because, whereas intracellular endosymbionts are widespread in both unicellular and multicellular eukaryotes (e.g. rhizobial bacteria, Chlorella cells i...

The phylogenetic position of the glaucophyte algae within the eukaryotic supergroup Plantae remains to be unambiguously established. Here, we assembled a multigene data set of conserved nuclear-encoded plastid-targeted proteins of cyanobacterial origin (i.e., through primary endosymbiotic gene transfer) from glaucophyte, red, and green (including l...

Here we use phylogenomics with expressed sequence tag (EST) data from the ecologically important coccolithophore-forming alga Emiliania huxleyi and the plastid-lacking cryptophyte Goniomonas cf. pacifica to establish their phylogenetic positions in the eukaryotic tree. Haptophytes and cryptophytes are members of the putative eukaryotic supergroup C...

The establishment of the photosynthetic organelle (plastid) in eukaryotes and the diversification of algae and plants were landmark evolutionary events because these taxa form the base of the food chain for many ecosystems on our planet. The plastid originated via a putative single, ancient primary endosymbiosis in which a heterotrophic protist eng...

A single cyanobacterial primary endosymbiosis that occurred approximately 1.5 billion years ago is believed to have given rise to the plastid in the common ancestor of the Plantae or Archaeplastida--the eukaryotic supergroup comprising red, green (including land plants), and glaucophyte algae. Critical to plastid establishment was the transfer of e...

Genomic data is accumulating in public database at an unprecedented rate. Although presently dominated by the sequences of metazoan, plant, parasitic, and picoeukaryotic taxa, both expressed sequence tag (EST) and complete genomes of free-living algae are also slowly appearing. This wealth of information offers the opportunity to clarify many long-...

The apicoplast is an essential organelle characteristic of the apicomplexan parasites. It harbors its own genome and it is believed to be a chloroplast-derived organelle that originated by secondary endosymbiosis. Here, we address the more relevant properties of this organelle, an evolutionary relict of a once fully-functional algal chloroplast. We...

The apicoplast is an essential organelle characteristic of the apicomplexan parasites. It harbors its own genome and it is believed to be a chloroplast-derived organelle that originated by secondary endosymbiosis. Here, we address the more relevant properties of this organelle, an evolutionary relict of a once fully-functional algal chloroplast. We...

Mitochondrial diseases display great diversity in clinical symptoms and biochemical characteristics. Although mtDNA mutations have been identified in many patients, there are currently no effective treatments. A number of human diseases result from mutations in mtDNA-encoded proteins, a group of proteins that are hydrophobic and have multiple membr...

Apicomplexans are parasites of great medical and veterinary importance. They contain a vestigial plastid, the apicoplast, that originated through the secondary endosymbiosis of the photosynthetic unicellular alga. The nature of this alga remains controversial. Here, we revisit the available evidence and critically summarize the "green vs. red" deba...

We suggested lateral transfer of split cox2a and cox2b genes from a chlorophyte algal ancestor to an apicomplexan ancestor ( [1][1] ). Waller et al. ( [2][2] ) oppose this interpretation based on a phylogeny implying close affiliation of apicomplexan cox2a and cox2b genes with ciliate cox2

Apicomplexan parasites, including the human pathogens Toxoplasma and Plasmodium , contain a vestigial plastid, the apicoplast. This chloroplast-derived organelle is the remnant of a secondary endosymbiosis between an ancestral apicomplexan and a photosynthetic organism whose origin is moot ([1–4][

The presence of an alternative oxidase (AOX) in Polytomella sp., a colorless relative of Chlamydomonas reinhardtii, was explored. Oxygen uptake in Polytomella sp. mitochondria was inhibited by KCN (94%) or antimycin (96%), and the remaining cyanide-resistant respiration was not blocked by the AOX inhibitors salicylhydroxamic acid (SHAM) or n-propyl...

The presence of an alternative oxidase (AOX) in Polytomella sp., a colorless relative of Chlamydomonas reinhardtii, was explored. Oxygen uptake in Polytomella sp. mitochondria was inhibited by KCN (94%) or antimycin (96%), and the remaining cyanide-resistant respiration was not blocked by the AOX inhibitors salicylhydroxamic acid (SHAM) or n-propyl...

Transfer of mitochondrial genes to the nucleus in chlamydomonad algae: perspective for the allotopic expression of OX-PHOS proteins and future human therapies