Huan Qiu

Cyanophora paradoxa Genome Elucidates Origin of Photosynthesis in Algae and Plants

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 unique origin for the plastid in the ancestor of this supergroup, which retains much of the ancestral diversity in genes involved in carbohydrate metabolism and fermentation, as well as in the gene content of the mitochondrial genome. Moreover, about 3.3% of nuclear genes in C. paradoxa seem to carry a signal of cyanobacterial ancestry, and key genes involved in starch biosynthesis are derived from energy parasites such as Chlamydiae. Rapid radiation, reticulate evolution via horizontal gene transfer, high rates of gene divergence, loss, and replacement, may have diffused the evolutionary signals within this supergroup, which perhaps explains previous difficulties in resolving its evolutionary history. An ancient algal genome suggests a unique origin of the plastid in the ancestor to plants, algae, and glaucophytes. 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 retains ancestral features of starch biosynthesis, fermentation, and plastid protein translocation common to plants and algae but lacks typical eukaryotic light-harvesting complex proteins. Traces of an ancient link to parasites such as Chlamydiae were found in the genomes of C. paradoxa and other Plantae. Apparently, Chlamydia-like bacteria donated genes that allow export of photosynthate from the plastid and its polymerization into storage polysaccharide in the cytosol.

Genome of the red alga Porphyridium purpureum

The limited knowledge we have about red algal genomes comes from the highly specialized extremophiles, Cyanidiophyceae. Here, we describe the first genome sequence from a mesophilic, unicellular red alga, Porphyridium purpureum. The 8,355 predicted genes in P. purpureum, hundreds of which are likely to be implicated in a history of horizontal gene transfer, reside in a genome of 19.7 Mbp with 235 spliceosomal introns. Analysis of light-harvesting complex proteins reveals a nuclear-encoded phycobiliprotein in the alga. We uncover a complex set of carbohydrate-active enzymes, identify the genes required for the methylerythritol phosphate pathway of isoprenoid biosynthesis, and find evidence of sexual reproduction. Analysis of the compact, function-rich genome of P. purpureum suggests that ancestral lineages of red algae acted as mediators of horizontal gene transfer between prokaryotes and photosynthetic eukaryotes, thereby significantly enriching genomes across the tree of photosynthetic life.

Comparative genomics explains the evolutionary success of reef-forming corals

Transcriptome and genome data from twenty stony coral species and a selection of reference bilaterians were studied to elucidate coral evolutionary history. We identified genes that encode the proteins responsible for the precipitation and aggregation of the aragonite skeleton on which the organisms live, and revealed a network of environmental sensors that coordinate responses of the host animals to temperature, light, and pH. Furthermore, we describe a variety of stress-related pathways, including apoptotic pathways that allow the host animals to detoxify reactive oxygen and nitrogen species that are generated by their intracellular photosynthetic symbionts, and determine the fate of corals under environmental stress. Some of these genes arose through horizontal gene transfer and comprise at least 0.2% of the animal gene inventory. Our analysis elucidates the evolutionary strategies that have allowed symbiotic corals to adapt and thrive for hundreds of millions of years. DOI: http://dx.doi.org/10.7554/eLife.13288.001

Adaptation through horizontal gene transfer in the cryptoendolithic red alga Galdieria phlegrea

Summary Thriving in the hot, acidic, and metal-rich environments associated with geothermal areas is possible for only a few eukaryotes, with the Cyanidiophytina red algae ( Cyanidium , Galdieria , and Cyanidioschyzon ) being a famous example. These unicellular taxa can live in pH 0–4 and temperatures reaching up to 56°C [1,2]. Because Cyanidiophytina is sister to a vast array of mesophilic red algae (the Rhodophytina), such as the unicellular Porphyridium and the seaweed Chondrus [3], the genetic basis of their adaptation to extreme environments is of great interest from both the perspective of biotechnology and of evolution. The recently completed 13.7 Mbp genome sequence from the hot-spring dwelling Galdieria sulphuraria demonstrated that horizontal gene transfer (HGT) from prokaryotic sources provided this taxon with remarkable metabolic versatility ( e.g ., glycerol metabolism) and the ability to survive in its hostile environment ( e.g. , genes to detoxify mercury and arsenic) [4]. To explore the role of HGT in other members of this genus, we generated an 11.4 Mbp draft genome assembly from the sister taxon G. phlegrea DBV 009 [5]. In contrast to G. sulphuraria, this species is adapted to dry habitats near fumaroles such as fissures between rocks or cryptoendolithic environments [5,6]. Here, we provide evidence for extensive gene loss in the common ancestor of Cyanidiophytina that includes the eukaryote-derived loci required for urea utilization. Surprisingly, we find that G. phlegrea has regained the complete set of genes required for urea hydrolysis through HGT from eubacteria. The unlinked nature of these genes is likely explained by multiple gene transfers that resulted in assembly of the pathway in G . phlegrea . Our study demonstrates that genome reduction, a common outcome in eukaryotes for adaptation to a specialized niche, can be ameliorated by the gain of once lost, or novel functions through HGT.

Genome of the halotolerant green alga Picochlorum sp. reveals strategies for thriving under fluctuating environmental conditions

An expected outcome of climate change is intensification of the global water cycle, which magnifies surface water fluxes, and consequently alters salinity patterns. It is therefore important to understand the adaptations and limits of microalgae to survive changing salinities. To this end, we sequenced the 13.5 Mbp genome of the halotolerant green alga Picochlorum SENEW3 (SE3) that was isolated from a brackish water pond subject to large seasonal salinity fluctuations. Picochlorum SE3 encodes 7367 genes, making it one of the smallest and most gene dense eukaryotic genomes known. Comparison with the pico-prasinophyte Ostreococcus tauri, a species with a limited range of salt tolerance, reveals the enrichment of transporters putatively involved in the salt stress response in Picochlorum SE3. Analysis of cultures and the protein complement highlight the metabolic flexibility of Picochlorum SE3 that encodes genes involved in urea metabolism, acetate assimilation and fermentation, acetoin production and glucose uptake, many of which form functional gene clusters. Twenty-four cases of horizontal gene transfer from bacterial sources were found in Picochlorum SE3 with these genes involved in stress adaptation including osmolyte production and growth promotion. Our results identify Picochlorum SE3 as a model for understanding microalgal adaptation to stressful, fluctuating environments.

Evidence of ancient genome reduction in red algae (Rhodophyta).

Red algae (Rhodophyta) comprise a monophyletic eukaryotic lineage of ~6,500 species with a fossil record that extends back 1.2 billion years. A surprising aspect of red algal evolution is that sequenced genomes encode a relatively limited gene inventory (~5–10 thousand genes) when compared with other free‐living algae or to other eukaryotes. This suggests that the common ancestor of red algae may have undergone extensive genome reduction, which can result from lineage specialization to a symbiotic or parasitic lifestyle or adaptation to an extreme or oligotrophic environment. We gathered genome and transcriptome data from a total of 14 red algal genera that represent the major branches of this phylum to study genome evolution in Rhodophyta. Analysis of orthologous gene gains and losses identifies two putative major phases of genome reduction: (i) in the stem lineage leading to all red algae resulting in the loss of major functions such as flagellae and basal bodies, the glycosyl‐phosphatidylinositol anchor biosynthesis pathway, and the autophagy regulation pathway; and (ii) in the common ancestor of the extremophilic Cyanidiophytina. Red algal genomes are also characterized by the recruitment of hundreds of bacterial genes through horizontal gene transfer that have taken on multiple functions in shared pathways and have replaced eukaryotic gene homologs. Our results suggest that Rhodophyta may trace their origin to a gene depauperate ancestor. Unlike plants, it appears that a limited gene inventory is sufficient to support the diversification of a major eukaryote lineage that possesses sophisticated multicellular reproductive structures and an elaborate triphasic sexual cycle.

Phylogenomic analysis uncovers the evolutionary history of nutrition and infection mode in rice blast fungus and other Magnaporthales

The order Magnaporthales (Ascomycota, Fungi) includes devastating pathogens of cereals, such as the rice blast fungus Pyricularia (Magnaporthe) oryzae, which is a model in host-pathogen interaction studies. Magnaporthales also includes saprotrophic species associated with grass roots and submerged wood. Despite its scientific and economic importance, the phylogenetic position of Magnaporthales within Sordariomycetes and the interrelationships of its constituent taxa, remain controversial. In this study, we generated novel transcriptome data from 21 taxa that represent key Magnaporthales lineages of different infection and nutrition modes and phenotypes. Phylogenomic analysis of >200 conserved genes allowed the reconstruction of a robust Sordariomycetes tree of life that placed the monophyletic group of Magnaporthales sister to Ophiostomatales. Among Magnaporthales, three major clades were recognized: 1) an early diverging clade A comprised of saprotrophs associated with submerged woods; 2) clade B that includes the rice blast fungus and other pathogens that cause blast diseases of monocot plants. These species infect the above-ground tissues of host plants using the penetration structure, appressorium; and 3) clade C comprised primarily of root-associated species that penetrate the root tissue with hyphopodia. The well-supported phylogenies provide a robust framework for elucidating evolution of pathogenesis, nutrition modes, and phenotypic characters in Magnaporthales.

Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta)

Significance Fossil evidence shows that red algae (Rhodophyta) are one of the most ancient multicellular lineages. Their ecological, evolutionary, and commercial importance notwithstanding, few red algal nuclear genomes have been sequenced. Our analyses of the Porphyra umbilicalis genome provide insights into how this macrophyte thrives in the stressful intertidal zone and into the basis for its nutritional value as human food. Many of the novel traits (e.g., cytoskeletal organization, calcium signaling pathways) we find encoded in the Porphyra genome are extended to other red algal genomes, and our unexpected findings offer a potential explanation for why the red algae are constrained to small stature relative to other multicellular lineages. Porphyra umbilicalis (laver) belongs to an ancient group of red algae (Bangiophyceae), is harvested for human food, and thrives in the harsh conditions of the upper intertidal zone. Here we present the 87.7-Mbp haploid Porphyra genome (65.8% G + C content, 13,125 gene loci) and elucidate traits that inform our understanding of the biology of red algae as one of the few multicellular eukaryotic lineages. Novel features of the Porphyra genome shared by other red algae relate to the cytoskeleton, calcium signaling, the cell cycle, and stress-tolerance mechanisms including photoprotection. Cytoskeletal motor proteins in Porphyra are restricted to a small set of kinesins that appear to be the only universal cytoskeletal motors within the red algae. Dynein motors are absent, and most red algae, including Porphyra, lack myosin. This surprisingly minimal cytoskeleton offers a potential explanation for why red algal cells and multicellular structures are more limited in size than in most multicellular lineages. Additional discoveries further relating to the stress tolerance of bangiophytes include ancestral enzymes for sulfation of the hydrophilic galactan-rich cell wall, evidence for mannan synthesis that originated before the divergence of green and red algae, and a high capacity for nutrient uptake. Our analyses provide a comprehensive understanding of the red algae, which are both commercially important and have played a major role in the evolution of other algal groups through secondary endosymbioses.

Extensive horizontal gene transfers between plant pathogenic fungi

BackgroundHorizontal gene transfer (HGT) plays an important role in the adaptation of lineages to changing environments. The extent of this process in eukaryotes, however, remains controversial. The most well-known and dramatic form of HGT represents intracellular gene transfer from endosymbionts to the host nuclear genome. Such episodes of transfer typically involve hundreds of genes and are thought to be possible only in the case of endosymbiosis.ResultsUsing a conservative phylogenomic approach, we analyzed genomic data from the fungal pathogen Magnaporthiopsis incrustans in the order Magnaporthales and identified two instances of exclusive sharing of HGT-derived gene markers between Magnaporthales and another lineage of plant-pathogenic fungi in the genus Colletotrichum. Surprisingly, inspection of these data demonstrated that HGT is far more widespread than anticipated, with more than 90 genes (including 33 highly supported candidates) being putatively transferred between Magnaporthales and Colletotrichum. These gene transfers are often physically linked in the genome and show more than two-fold functional enrichment in carbohydrate activating enzymes associated with plant cell wall degradation.ConclusionsOur work provides a novel perspective on the scale of HGT between eukaryotes. These results challenge the notion that recognized HGT plays a minor role in the evolution of fungal lineages, and in the case we describe, is likely implicated in the evolution of plant pathogenesis. More generally, we suggest that the expanding database of closely related eukaryotic genomes and the application of novel analytic methods will further underline the significant impact of foreign gene acquisition across the tree of life. Major lifestyle transitions such as those accompanying the origin of extremophily or pathogenesis are expected to be ideal candidates for studying the mode and tempo of HGT.

Why we need more algal genomes

In the current post-genomics world, a relevant question on the minds of many phycologists might be: do we really need more algal genomes or, should we stop and focus on the hard job of developing genetic tools and other resources for already sequenced taxa? This question has, in our opinion, a clear answer: we need to do both. Here, we focus on the genome sequencing side and discuss the following reasons why we think algal (and related heterotrophic protist) genome sequencing should remain a focus of phycological research: (1) transcriptomes that aim to create gene inventories or study gene expression differences (primarily Illumina RNAseq data), although cheap to produce and relatively easy to analyze, may not be sufficient for in-depth study of genomes, (2) much of natural biodiversity is still unstudied, necessitating approaches such as single cell genomics (SCG) that, although still challenging when applied to algae, can sample taxa isolated directly from the environment, (3) horizontal gene transfer (HGT) in algae is no longer controversial, but rather a major contributor to the evolution of photosynthetic lineages, and its study benefits greatly from completed (or draft) genomes, and (4) epigenetics and genome evolution among populations are best studied using assembled genome data. The power of RNAseq data to support gene discovery and, in particular, gene expression differences is clearly very high and has been exploited by many groups including the large-scale Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP; Keeling et al. 2014; http://marinemicroeukaryotes.org/) and the 1,000 Plants (1KP; http://onekp.com/project.html) initiative and an array of more focused studies. These data provide significant opportunities for phycologists and are (still) the most appropriate approach for groups such as dinoflagellates that have enormous nuclear genomes that may be several times the size in humans (e.g., Hou and Lin 2009). Nonetheless, the benefits of RNAseq data can be greatly improved with the availability of reference genomes to build more accurate and complete gene models and to discriminate between nuclear “host” and contaminant genes. Whole genome analysis and annotation also provide information about gene structure (e.g., intron number and distribution; Nakamura et al. 2013), transposons (Read et al. 2013), and gene synteny (Blanc et al. 2012) that is invaluable for interpreting molecular evolution. In addition, sole use of transcriptome sequences may lead to assembly artifacts resulting in inflated gene counts and false contigs. This is partly explained by the significant coverage variation in assembled cDNA data that reflects gene expression differences across coding regions. This aspect, when compounded with sequencing errors in “over sequenced” areas can result in a poor or fragmented assembly (for discussion, see Martin and Wang 2011). In contrast, gene models predicted using complementary RNAseq and genome data generally provide a more complete and accurate inventory of nuclear genes, in particular, in identifying gene start and stop sites. Work with Porphyridium purpureum (Rhodophyta) showed that high quality RNAseq data alone identified 36,167 unique assembled contigs (N50 = 1,298nt), whereas only 8,355 genes were predicted in the genome. No obvious evidence of alternative splicing was found as an explanation for the high number of RNAseq-derived contigs in this red alga (Bhattacharya et al. 2013). Similarly, Shoguchi et al. (2013) assembled 63,104 unique RNAseq-derived contigs (N50 = 1,586nt) in a study of the coral symbiont Symbiodinium minutum (Dinophyceae), a genome that encodes ~42K genes. Therefore, genome data and the resulting gene models are the fundamental unit of study for many scientists and are used to provide templates for synthetic gene construction (Rockwell et al. 2014), to understand protein targeting (i.e., the N-terminus is needed for this purpose; Emanuelsson et al. 2000), to determine accurately gene family size (e.g., pherophorins in Volvox carteri; Prochnik et al. 2010), to have a reliable reference to map cDNA transcripts Received 22 August 2014. Accepted 10 November 2014. Author for correspondence: e-mail bhattacharya@aesop.rutgers.edu. Editorial Responsibility: M. Graham (Managing Editor) J. Phycol. 51, 1–5 (2015)