scholarly journals Tightly constrained genome reduction and relaxation of purifying selection during secondary plastid endosymbiosis

2021 ◽  
Author(s):  
Kavitha Uthanumallian ◽  
Cintia Iha ◽  
Sonja I Repetti ◽  
Cheong Xin Chan ◽  
Debashish Bhattacharya ◽  
...  
Keyword(s):  
Gene Loss ◽  
Purifying Selection ◽  
Eukaryotic Cell ◽  
Secondary Endosymbiosis ◽  
Molecular Processes ◽  
Free Living ◽  
Plastid Genomes ◽  
Secondary Plastid ◽  
Photosynthetic Eukaryotes ◽  
Secondary Plastids

Abstract Endosymbiosis, the establishment of a former free-living prokaryotic or eukaryotic cell as an organelle inside a host cell, can dramatically alter the genomic architecture of the endosymbiont. Plastids or chloroplasts, the light-harvesting organelle of photosynthetic eukaryotes, are excellent models to study this phenomenon because plastid origin has occurred multiple times in evolution. Here, we investigate the genomic signature of molecular processes acting through secondary plastid endosymbiosis—the origination of a new plastid from a free-living eukaryotic alga. We used phylogenetic comparative methods to study gene loss and changes in selective regimes on plastid genomes, focusing on green algae that have given rise to three independent lineages with secondary plastids (euglenophytes, chlorarachniophytes, and Lepidodinium). Our results show an overall increase in gene loss associated with secondary endosymbiosis, but this loss is tightly constrained by retention of genes essential for plastid function. The data show that secondary plastids have experienced temporary relaxation of purifying selection during secondary endosymbiosis. However, this process is tightly constrained, with selection relaxed only relative to the background in primary plastids. Purifying selection remains strong in absolute terms even during the endosymbiosis events. Selection intensity rebounds to pre-endosymbiosis levels following endosymbiosis events, demonstrating the changes in selection efficiency during different origin phases of secondary plastids. Independent endosymbiosis events in the euglenophytes, chlorarachniophytes, and Lepidodinium differ in their degree of relaxation of selection, highlighting the different evolutionary contexts of these events. This study reveals the selection-drift interplay during secondary endosymbiosis, and evolutionary parallels during organellogenesis.

scholarly journals Factors mediating plastid dependency and the origins of parasitism in apicomplexans and their close relatives

2015 ◽  
Vol 112 (33) ◽  
pp. 10200-10207 ◽  
Author(s):  
Jan Janouškovec ◽  
Denis V. Tikhonenkov ◽  
Fabien Burki ◽  
Alexis T. Howe ◽  
Martin Kolísko ◽  
...  
Keyword(s):  
Plastid Genome ◽  
Sequence Data ◽  
Sister Group ◽  
Molecular Characteristics ◽  
Phylogenomic Analysis ◽  
Free Living ◽  
Plastid Genomes ◽  
Monophyletic Lineage ◽  
Causative Agents ◽  
Close Relatives

Apicomplexans are a major lineage of parasites, including causative agents of malaria and toxoplasmosis. How such highly adapted parasites evolved from free-living ancestors is poorly understood, particularly because they contain nonphotosynthetic plastids with which they have a complex metabolic dependency. Here, we examine the origin of apicomplexan parasitism by resolving the evolutionary distribution of several key characteristics in their closest free-living relatives, photosynthetic chromerids and predatory colpodellids. Using environmental sequence data, we describe the diversity of these apicomplexan-related lineages and select five species that represent this diversity for transcriptome sequencing. Phylogenomic analysis recovered a monophyletic lineage of chromerids and colpodellids as the sister group to apicomplexans, and a complex distribution of retention versus loss for photosynthesis, plastid genomes, and plastid organelles. Reconstructing the evolution of all plastid and cytosolic metabolic pathways related to apicomplexan plastid function revealed an ancient dependency on plastid isoprenoid biosynthesis, predating the divergence of apicomplexan and dinoflagellates. Similarly, plastid genome retention is strongly linked to the retention of two genes in the plastid genome, sufB and clpC, altogether suggesting a relatively simple model for plastid retention and loss. Lastly, we examine the broader distribution of a suite of molecular characteristics previously linked to the origins of apicomplexan parasitism and find that virtually all are present in their free-living relatives. The emergence of parasitism may not be driven by acquisition of novel components, but rather by loss and modification of the existing, conserved traits.

scholarly journals Rampant Nuclear Transfer and Substitutions of Plastid Genes in Passiflora

2020 ◽  
Vol 12 (8) ◽  
pp. 1313-1329 ◽  
Author(s):  
Bikash Shrestha ◽  
Lawrence E Gilbert ◽  
Tracey A Ruhlman ◽  
Robert K Jansen
Keyword(s):  
Nuclear Transfer ◽  
Protein Complexes ◽  
Nuclear Gene ◽  
Transit Peptide ◽  
Purifying Selection ◽  
Rna Recognition Motif ◽  
Rna Recognition ◽  
Plastid Genomes ◽  
Type Gene ◽  
Conserved Gene

Abstract Gene losses in plastid genomes (plastomes) are often accompanied by functional transfer to the nucleus or substitution of an alternative nuclear-encoded gene. Despite the highly conserved gene content in plastomes of photosynthetic land plants, recent gene loss events have been documented in several disparate angiosperm clades. Among these lineages, Passiflora lacks several essential ribosomal genes, rps7, rps16, rpl20, rpl22, and rpl32, the two largest plastid genes, ycf1 and ycf2, and has a highly divergent rpoA. Comparative transcriptome analyses were performed to determine the fate of the missing genes in Passiflora. Putative functional transfers of rps7, rpl22, and rpl32 to nucleus were detected, with the nuclear transfer of rps7, representing a novel event in angiosperms. Plastid-encoded rps7 was transferred into the intron of a nuclear-encoded plastid-targeted thioredoxin m-type gene, acquiring its plastid transit peptide (TP). Plastid rpl20 likely experienced a novel substitution by a duplicated, nuclear-encoded mitochondrial-targeted rpl20 that has a similar gene structure. Additionally, among rosids, evidence for a third independent transfer of rpl22 in Passiflora was detected that gained a TP from a nuclear gene containing an organelle RNA recognition motif. Nuclear transcripts representing rpoA, ycf1, and ycf2 were not detected. Further analyses suggest that the divergent rpoA remains functional and that the gene is under positive or purifying selection in different clades. Comparative analyses indicate that alternative translocon and motor protein complexes may have substituted for the loss of ycf1 and ycf2 in Passiflora.

scholarly journals Unprecedented Parallel Photosynthetic Losses in a Heterotrophic Orchid Genus

2019 ◽  
Vol 36 (9) ◽  
pp. 1884-1901 ◽  
Author(s):  
Craig F Barrett ◽  
Brandon T Sinn ◽  
Aaron H Kennedy
Keyword(s):  
Genome Evolution ◽  
Gene Loss ◽  
Photosynthetic Apparatus ◽  
Housekeeping Genes ◽  
Genomic Rearrangements ◽  
Model Organisms ◽  
Plastid Genomes ◽  
Genome Modification ◽  
Single Genus ◽  
Genome Degradation

AbstractHeterotrophic plants are evolutionary experiments in genomic, morphological, and physiological change. Yet, genomic sampling gaps exist among independently derived heterotrophic lineages, leaving unanswered questions about the process of genome modification. Here, we have sequenced complete plastid genomes for all species of the leafless orchid genus Hexalectris, including multiple individuals for most, and leafy relatives Basiphyllaea and Bletia. Our objectives are to determine the number of independent losses of photosynthesis and to test hypotheses on the process of genome degradation as a result of relaxed selection. We demonstrate four to five independent losses of photosynthesis in Hexalectris based on degradation of the photosynthetic apparatus, with all but two species displaying evidence of losses, and variation in gene loss extending below the species level. Degradation in the atp complex is advanced in Hexalectris warnockii, whereas only minimal degradation (i.e., physical loss) has occurred among some “housekeeping” genes. We find genomic rearrangements, shifts in Inverted Repeat boundaries including complete loss in one accession of H. arizonica, and correlations among substitutional and genomic attributes. Our unprecedented finding of multiple, independent transitions to a fully mycoheterotrophic lifestyle in a single genus reveals that the number of such transitions among land plants is likely underestimated. This study underscores the importance of dense taxon sampling, which is highly informative for advancing models of genome evolution in heterotrophs. Mycoheterotrophs such as Hexalectris provide forward-genetic opportunities to study the consequences of radical genome evolution beyond what is possible with mutational studies in model organisms alone.

scholarly journals A single loss of photosynthesis in diatoms

2018 ◽  
Author(s):  
Anastasiia Onyshchenko ◽  
Elizabeth C. Ruck ◽  
Teofil Nakov ◽  
Andrew J. Alverson
Keyword(s):  
Plastid Genome ◽  
Phylogenetic Diversity ◽  
Phylogenetic Analyses ◽  
Rare Event ◽  
Small Subset ◽  
Plastid Genomes ◽  
Photosynthetic Eukaryotes ◽  
Large Numbers ◽  
Group A ◽  
The Common

AbstractLoss of photosynthesis is a common and often repeated trajectory in nearly all major groups of photosynthetic eukaryotes. One small subset of ‘apochloritic’ diatoms in the genus Nitzschia have lost their ability to photosynthesize and require extracellular carbon for growth. Similar to other secondarily nonphotosynthetic taxa, apochloritic diatoms maintain colorless plastids with highly reduced plastid genomes. Although the narrow taxonomic breadth of apochloritic diatoms suggests a single loss of photosynthesis in the common ancestor of these species, previous phylogenetic analyses suggested that photosynthesis was lost multiple times. We sequenced additional phylogenetic markers from the nuclear and mitochondrial genomes for a larger set of taxa and found that the best trees for datasets representing all three genetic compartments provided low to moderate support for monophyly of apochloritic Nitzschia, consistent with a single loss of photosynthesis in diatoms. We sequenced the plastid genome of one apochloritic species and found that it was highly similar in all respects to the plastid genome of another apochloritic Nitzschia species, indicating that streamlining of the plastid genome had completed prior to the split of these two species. Finally, it is increasingly clear that some locales host relatively large numbers apochloritic Nitzschia species that span the phylogenetic diversity of the group, indicating that these species co-exist because of resource abundance or resource partitioning in ecologically favorable habitats. A better understanding of the phylogeny and ecology of this group, together with emerging genomic resources, will help identify the factors that have driven and maintained the loss of photosynthesis in this group, a rare event in diatoms.

scholarly journals Mechanisms Driving Genome Reduction of a Novel Roseobacter Lineage Showing Vitamin B12 Auxotrophy

2021 ◽  
Author(s):  
Xiaoyuan Feng ◽  
Xiao Chu ◽  
Yang Qian ◽  
Michael W. Henson ◽  
V. Celeste Lanclos ◽  
...  
Keyword(s):  
Purifying Selection ◽  
Genome Reduction ◽  
Vitamin B ◽  
Free Living ◽  
Signature Genes ◽  
Genome Content ◽  
Ecological Transition ◽  
Globally Distributed ◽  
Global Carbon ◽  
Gene Expression Levels

SummaryMembers of the marine Roseobacter group are key players in the global carbon and sulfur cycles. While over 300 species have been described, only 2% possess reduced genomes (mostly 3-3.5 Mbp) compared to an average roseobacter (>4 Mbp). These taxonomic minorities are phylogenetically diverse but form a Pelagic Roseobacter Cluster (PRC) at the genome content level. Here, we cultivated eight isolates constituting a novel Roseobacter lineage which we named ‘CHUG’. Metagenomic and metatranscriptomic read recruitment analyses showed that CHUG members were globally distributed and active in marine environments. CHUG members possess some of the smallest genomes (~2.52 Mb) among all known roseobacters, but they do not exhibit canonical features of genome streamlining like higher coding density or fewer paralogues and pseudogenes compared to their sister lineages. While CHUG members are clustered with traditional PRC members at the genome content level, they show important differences. Unlike other PRC members, neither the relative abundances of CHUG members nor their gene expression levels are correlated with chlorophyll a concentration across the global samples. Moreover, CHUG members cannot synthesize vitamin B12, a key metabolite made by most roseobacters but not by many phytoplankton species and thus thought to mediate the roseobacter-phytoplankton interactions. This combination of features is evidence for the hypothesis that CHUG members may have evolved a free-living lifestyle decoupled from phytoplankton. This ecological transition was accompanied by the loss of signature genes involved in roseobacter-phytoplankton symbiosis, suggesting that relaxation of purifying selection is likely an important driver of genome reduction in CHUG.

scholarly journals Organelle Studies and Proteome Analyses of Mitochondria and Plastids Fractions from the Diatom Thalassiosira pseudonana

2019 ◽  
Vol 60 (8) ◽  
pp. 1811-1828 ◽  
Author(s):  
Alexander F Schober ◽  
Carolina R�o B�rtulos ◽  
Annsophie Bischoff ◽  
Bernard Lepetit ◽  
Ansgar Gruber ◽  
...  
Keyword(s):  
Mass Spectrometry ◽  
Mitochondrial Respiration ◽  
Eukaryotic Cell ◽  
Thalassiosira Pseudonana ◽  
Ionization Mass ◽  
Secondary Endosymbiosis ◽  
Western Blots ◽  
Unicellular Algae ◽  
In Organello ◽  
Complex Architecture

Abstract Diatoms are unicellular algae and evolved by secondary endosymbiosis, a process in which a red alga-like eukaryote was engulfed by a heterotrophic eukaryotic cell. This gave rise to plastids of remarkable complex architecture and ultrastructure that require elaborate protein importing, trafficking, signaling and intracellular cross-talk pathways. Studying both plastids and mitochondria and their distinctive physiological pathways in organello may greatly contribute to our understanding of photosynthesis, mitochondrial respiration and diatom evolution. The isolation of such complex organelles, however, is still demanding, and existing protocols are either limited to a few species (for plastids) or have not been reported for diatoms so far (for mitochondria). In this work, we present the first isolation protocol for mitochondria from the model diatom Thalassiosira pseudonana. Apart from that, we extended the protocol so that it is also applicable for the purification of a high-quality plastids fraction, and provide detailed structural and physiological characterizations of the resulting organelles. Isolated mitochondria were structurally intact, showed clear evidence of mitochondrial respiration, but the fractions still contained residual cell fragments. In contrast, plastid isolates were virtually free of cellular contaminants, featured structurally preserved thylakoids performing electron transport, but lost most of their stromal components as concluded from Western blots and mass spectrometry. Liquid chromatography electrospray-ionization mass spectrometry studies on mitochondria and thylakoids, moreover, allowed detailed proteome analyses which resulted in extensive proteome maps for both plastids and mitochondria thus helping us to broaden our understanding of organelle metabolism and functionality in diatoms.

scholarly journals Global genome analysis of the shikimic acid pathway reveals greater gene loss in host-associated than in free-living bacteria

BMC Genomics ◽  
2010 ◽  
Vol 11 (1) ◽  
Author(s):  
Jurica Zucko ◽  
Walter C Dunlap ◽  
J Malcolm Shick ◽  
John Cullum ◽  
François Cercelet ◽  
...  
Keyword(s):  
Genome Analysis ◽  
Gene Loss ◽  
Shikimic Acid ◽  
Free Living ◽  
Shikimic Acid Pathway ◽  
Acid Pathway ◽  
Living Bacteria

scholarly journals The Naegleria genome: a free-living microbial eukaryote lends unique insights into core eukaryotic cell biology

2011 ◽  
Vol 162 (6) ◽  
pp. 607-618 ◽  
Author(s):  
Lillian K. Fritz-Laylin ◽  
Michael L. Ginger ◽  
Charles Walsh ◽  
Scott C. Dawson ◽  
Chandler Fulton
Keyword(s):  
Cell Biology ◽  
Eukaryotic Cell ◽  
Free Living ◽  
Microbial Eukaryote

scholarly journals The origin of plastids

2008 ◽  
Vol 363 (1504) ◽  
pp. 2675-2685 ◽  
Author(s):  
C.J Howe ◽  
A.C Barbrook ◽  
R.E.R Nisbet ◽  
P.J Lockhart ◽  
A.W.D Larkum
Keyword(s):  
Recent Work ◽  
Discrete Time ◽  
Sequence Data ◽  
Phylogenetic Reconstruction ◽  
Taxon Sampling ◽  
Photosynthetic Eukaryote ◽  
Bag Model ◽  
Monophyletic Origin ◽  
Photosynthetic Eukaryotes ◽  
Secondary Plastids

It is generally accepted that plastids first arose by acquisition of photosynthetic prokaryotic endosymbionts by non-photosynthetic eukaryotic hosts. It is also accepted that photosynthetic eukaryotes were acquired on several occasions as endosymbionts by non-photosynthetic eukaryote hosts to form secondary plastids. In some lineages, secondary plastids were lost and new symbionts were acquired, to form tertiary plastids. Most recent work has been interpreted to indicate that primary plastids arose only once, referred to as a ‘monophyletic’ origin. We critically assess the evidence for this. We argue that the combination of Ockham's razor and poor taxon sampling will bias studies in favour of monophyly. We discuss possible concerns in phylogenetic reconstruction from sequence data. We argue that improved understanding of lineage-specific substitution processes is needed to assess the reliability of sequence-based trees. Improved understanding of the timing of the radiation of present-day cyanobacteria is also needed. We suggest that acquisition of plastids is better described as the result of a process rather than something occurring at a discrete time, and describe the ‘shopping bag’ model of plastid origin. We argue that dinoflagellates and other lineages provide evidence in support of this.

scholarly journals Gene loss on Y chromosomes: a consequence of purifying selection?

Fly ◽  
2010 ◽  
Vol 4 (4) ◽  
pp. 270-272 ◽  
Author(s):  
Vera B. Kaiser
Keyword(s):  
Gene Loss ◽  
Purifying Selection ◽  
Y Chromosomes
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