Origin and Evolution of Plastids and Photosynthesis in Eukaryotes

Recent progress in understanding the origins of plastids from endosymbiotic cyanobacteria is reviewed. Establishing when during geological time the endosymbiosis occurred remains elusive, but progress has been made in defining the cyanobacterial lineage most closely related to plastids, and some mechanistic insight into the possible existence of cryptic endosymbioses perhaps involving Chlamydia-like infections of the host have also been presented. The phylogenetic affinities of the host remain obscure. The existence of a second lineage of primary plastids in euglyphid amoebae has now been confirmed, but the quasipermanent acquisition of plastids by animals has been shown to be more ephemeral than initially suspected. A new understanding of how plastids have been integrated into their hosts by transfer of photosynthate, by endosymbiotic gene transfer and repatriation of gene products back to the endosymbiont, and by regulation of endosymbiont division is presented in context.Photosynthesis is biology’s equivalent of alchemy converting a common substance (CO₂) into a precious one (reduced carbon compounds rich in chemical energy). Freely available light energy is initially converted to precious chemical energy in the form of ATP. This energy, and the reducing power generated by splitting water molecules to release electrons, is used to fix carbon from atmospheric CO₂ and generate reduced carbon compounds that underpin the biosphere. It is estimated that plants and algae convert 258 billion tons of carbon dioxide into biomass by photosynthesis annually (Geider et al. 2001). Microfossils in ancient stromatolites indicate that cyanobacterium-like organisms had invented this process—or an early, perhaps nonoxygenic, version of it—at least 3.5 byo (billions of years old) (Lowe 1980; Walter et al. 1980; Schopf 1993). These photosynthetic prokaryotes substantially predate eukaryotes, which emerged much later (Rasmussen et al. 2008; Koonin 2010). The common ancestor of all eukaryotes entered into an endosymbiotic partnership with an α-proteobacterium that evolved into the mitochondrion, now the site of aerobic respiration in most eukaryotes (Gray 2012); animals and fungi are heterotrophic descendants of this partnership. Another lineage, which eventually produced the plants, entered into a second endosymbiotic partnership, this time with a cyanobacterium, which transplanted photosynthetic alchemy into eukaryotes to create plastids (Gray and Archibald 2012). This review will highlight recent progress in our understanding of the origin and evolution of plastids.     

Biochemistry and Evolution of Anaerobic Energy Metabolism in Eukaryotes

Summary: Major insights into the phylogenetic distribution, biochemistry, and evolutionary significance of organelles involved in ATP synthesis (energy metabolism) in eukaryotes that thrive in anaerobic environments for all or part of their life cycles have accrued in recent years. All known eukaryotic groups possess an organelle of mitochondrial origin, mapping the origin of mitochondria to the eukaryotic common ancestor, and genome sequence data are rapidly accumulating for eukaryotes that possess anaerobic mitochondria, hydrogenosomes, or mitosomes. Here we review the available biochemical data on the enzymes and pathways that eukaryotes use in anaerobic energy metabolism and summarize the metabolic end products that they generate in their anaerobic habitats, focusing on the biochemical roles that their mitochondria play in anaerobic ATP synthesis. We present metabolic maps of compartmentalized energy metabolism for 16 well-studied species. There are currently no enzymes of core anaerobic energy metabolism that are specific to any of the six eukaryotic supergroup lineages; genes present in one supergroup are also found in at least one other supergroup. The gene distribution across lineages thus reflects the presence of anaerobic energy metabolism in the eukaryote common ancestor and differential loss during the specialization of some lineages to oxic niches, just as oxphos capabilities have been differentially lost in specialization to anoxic niches and the parasitic life-style. Some facultative anaerobes have retained both aerobic and anaerobic pathways. Diversified eukaryotic lineages have retained the same enzymes of anaerobic ATP synthesis, in line with geochemical data indicating low environmental oxygen levels while eukaryotes arose and diversified.     

Evolution of DNA Replication Protein Complexes in Eukaryotes and Archaea

Background

The replication of DNA in Archaea and eukaryotes requires several ancillary complexes, including proliferating cell nuclear antigen (PCNA), replication factor C (RFC), and the minichromosome maintenance (MCM) complex. Bacterial DNA replication utilizes comparable proteins, but these are distantly related phylogenetically to their archaeal and eukaryotic counterparts at best.

Methodology/Principal Findings

While the structures of each of the complexes do not differ significantly between the archaeal and eukaryotic versions thereof, the evolutionary dynamic in the two cases does. The number of subunits in each complex is constant across all taxa. However, they vary subtly with regard to composition. In some taxa the subunits are all identical in sequence, while in others some are homologous rather than identical. In the case of eukaryotes, there is no phylogenetic variation in the makeup of each complex—all appear to derive from a common eukaryotic ancestor. This is not the case in Archaea, where the relationship between the subunits within each complex varies taxon-to-taxon. We have performed a detailed phylogenetic analysis of these relationships in order to better understand the gene duplications and divergences that gave rise to the homologous subunits in Archaea.

Conclusion/Significance

This domain level difference in evolution suggests that different forces have driven the evolution of DNA replication proteins in each of these two domains. In addition, the phylogenies of all three gene families support the distinctiveness of the proposed archaeal phylum Thaumarchaeota.     

A New Aspect to the Origin and Evolution of Eukaryotes

One of the most important omissions in recent evolutionary theory concerns how eukaryotes could emerge and evolve. According to the currently accepted views, the first eukaryotic cell possessed a nucleus, an endomembrane system, and a cytoskeleton but had an inefficient prokaryotic-like metabolism. In contrast, one of the most ancient eukaryotes, the metamonada Giardia lamblia, was found to have formerly possessed mitochondria. In sharp contrast with the traditional views, this paper suggests, based on the energetic aspect of genome organization, that the emergence of eukaryotes was promoted by the establishment of an efficient energy-converting organelle, such as the mitochondrion. Mitochondria were acquired by the endosymbiosis of ancient α-purple photosynthetic Gram-negative eubacteria that reorganized the prokaryotic metabolism of the archaebacterial-like ancestral host cells. The presence of an ATP pool in the cytoplasm provided by this cell organelle allowed a major increase in genome size. This evolutionary change, the remarkable increase both in genome size and complexity, explains the origin of the eukaryotic cell itself. The loss of cell wall and the appearance of multicellularity can also be explained by the acquisition of mitochondria. All bacteria use chemiosmotic mechanisms to harness energy; therefore the periplasm bounded by the cell wall is an essential part of prokaryotic cells. Following the establishment of mitochondria, the original plasma membrane-bound metabolism of prokaryotes, as well as the funcion of the periplasm providing a compartment for the formation of different ion gradients, has been transferred into the inner mitochondrial membrane and intermembrane space. After the loss of the essential function of periplasm, the bacterial cell wall could also be lost, which enabled the naked cells to establish direct connections among themselves. The relatively late emergence of mitochondria may be the reason why multicellularity evolved so slowly. Received: 29 May 1997 / Accepted: 9 October 1997     

Unearthing LTR Retrotransposon gag Genes Co-opted in the Deep Evolution of Eukaryotes

LTR retrotransposons comprise a major component of the genomes of eukaryotes. On occasion, retrotransposon genes can be recruited by their hosts for diverse functions, a process formally referred to as co-option. However, a comprehensive picture of LTR retrotransposon gag gene co-option in eukaryotes is still lacking, with several documented cases exclusively involving Ty3/Gypsy retrotransposons in animals. Here, we use a phylogenomic approach to systemically unearth co-option of retrotransposon gag genes above the family level of taxonomy in 2,011 eukaryotes, namely co-option occurring during the deep evolution of eukaryotes. We identify a total of 14 independent gag gene co-option events across more than 740 eukaryote families, eight of which have not been reported previously. Among these retrotransposon gag gene co-option events, nine, four, and one involve gag genes of Ty3/Gypsy, Ty1/Copia, and Bel-Pao retrotransposons, respectively. Seven, four, and three co-option events occurred in animals, plants, and fungi, respectively. Interestingly, two co-option events took place in the early evolution of angiosperms. Both selective pressure and gene expression analyses further support that these co-opted gag genes might perform diverse cellular functions in their hosts, and several co-opted gag genes might be subject to positive selection. Taken together, our results provide a comprehensive picture of LTR retrotransposon gag gene co-option events that occurred during the deep evolution of eukaryotes and suggest paucity of LTR retrotransposon gag gene co-option during the deep evolution of eukaryotes.     

The Evolution of Fatty Acid Desaturases and Cytochrome b5 in Eukaryotes

Desaturases that introduce double bonds into the fatty acids are involved in the adaptation of membrane fluidity to changes in the environment. Besides, polyunsaturated fatty acids (PUFAs) are increasingly recognized as important pharmaceutical and nutraceutical compounds. To successfully engineer organisms with increased stress tolerance or the ability to synthesize valuable PUFAs, detailed knowledge about the complexity of the desaturase family as well as understanding of the coevolution of desaturases and their cytochrome b5 electron donors is needed. We have constructed phylogenies of several hundred desaturase sequences from animals, plants, fungi and bacteria and of the cytochrome b5 domains that are fused to some of these enzymes. The analysis demonstrates the existence of three major desaturase acyl-CoA groups that share few similarities. Our results indicate that the fusion of Δ⁶-desaturase-like enzymes with their cytochrome b5 electron donor was a single event that took place in the common ancestor of all eukaryotes. We also propose the Δ⁶-desaturase-like enzymes as the most probable donor of the cytochrome b5 domain found in fungal Δ⁹-desaturases and argue that the recombination most likely happened soon after the separation of the animal and fungal ancestors. These findings answer some of the previously unresolved questions and contribute to the quickly expanding field of research on desaturases.     

Interactive Evolution Modules Promote Conceptual Change

We developed a suite of online modules () to improve student understanding of challenging concepts in our introductory biology course at the University of Wisconsin-Madison. Here we assess the effectiveness of two of the modules, Species and Speciation and Natural Selection. In Year 1, unannounced pre-tests and post-tests were used to assess students’ prior knowledge and any gains resulting from lecture attendance alone. Then to test the effectiveness of the modules we divided the class into three groups. Group 1 was assigned the interactive speciation module and their analysis of the final case study in the module was graded. Groups 2 and 3 were controls. In Group 1, the subgroup of students whose mean scores on the first two exams in the course were <80% scored an average of 10.5 percentage points better on exam 3, a significant improvement. In contrast, none of the other student groups showed significant improvements in their grades. In Year 2, we tested the effectiveness of the online modules when offered as optional, ungraded, activities. We again saw significant improvement (+3.8 percentage points) only in those students who completed the modules and whose averages on the previous two exams were <80%. The differences in improvement between years 1 and 2 suggest that it is not enough simply to provide students with tools that help them learn; they also need an incentive in the form of a grade or course credit to use the tools most effectively.     

原生动物的细胞骨架蛋白及其功能组件

目前在原生动物中发现了许多新的细胞骨架蛋白,如中心元蛋白、副鞭毛杆蛋白等。深入研究发现,原生动物的细胞骨架在细胞的模式形成,细胞核的遗传中也具有重要作用。从功能组件角度着眼研究细胞骨架的功能,将有助于了解细胞骨架的进化机制。     

Cytokinesis in Eukaryotes

Cytokinesis is the final event of the cell division cycle, and its completion results in irreversible partition of a mother cell into two daughter cells. Cytokinesis was one of the first cell cycle events observed by simple cell biological techniques; however, molecular characterization of cytokinesis has been slowed by its particular resistance to in vitro biochemical approaches. In recent years, the use of genetic model organisms has greatly advanced our molecular understanding of cytokinesis. While the outcome of cytokinesis is conserved in all dividing organisms, the mechanism of division varies across the major eukaryotic kingdoms. Yeasts and animals, for instance, use a contractile ring that ingresses to the cell middle in order to divide, while plant cells build new cell wall outward to the cortex. As would be expected, there is considerable conservation of molecules involved in cytokinesis between yeast and animal cells, while at first glance, plant cells seem quite different. However, in recent years, it has become clear that some aspects of division are conserved between plant, yeast, and animal cells. In this review we discuss the major recent advances in defining cytokinesis, focusing on deciding where to divide, building the division apparatus, and dividing. In addition, we discuss the complex problem of coordinating the division cycle with the nuclear cycle, which has recently become an area of intense research. In conclusion, we discuss how certain cells have utilized cytokinesis to direct development.     

On the Classification and Evolution of Protein Modules

Our efforts to classify the functional units of many proteins, the modules, are reviewed. The data from the sequencing projects for various model organisms are extremely helpful in deducing the evolution of proteins and modules. For example, a dramatic increase of modular proteins can be observed from yeast to C. elegans in accordance with new protein functions that had to be introduced in multicellular organisms. Our sequence characterization of modules relies on sensitive similarity search algorithms and the collection of multiple sequence alignments for each module. To trace the evolution of modules and to further automate the classification, we have developed a sequence and a module alerting system that checks newly arriving sequence data for the presence of already classified modules. Using these systems, we were able to identify an unexpected similarity between extracellular C1Q modules with bacterial proteins.     

Evolution of the 2′-5′-Oligoadenylate Synthetase Family in Eukaryotes and Bacteria

The 2′-5′-oligoadenylate synthetase (OAS) belongs to a nucleotidyl transferase family that includes poly(A) polymerases and CCA-adding enzymes. In mammals and birds, the OAS functions in the interferon system but it is also present in an active form in sponges, which are devoid of the interferon system. In view of these observations, we have pursued the idea that OAS genes could be present in other metazoans and in unicellular organisms as well. We have identified a number of OAS1 genes in annelids, mollusks, a cnidarian, chordates, and unicellular eukaryotes and also found a family of proteins in bacteria that contains the five OAS-specific motifs. This indicates a specific relationship to OAS. The wide distribution of the OAS genes has made it possible to suggest how the OAS1 gene could have evolved from a common ancestor to choanoflagellates and metazoans. Furthermore, we suggest that the OASL may have evolved from an ancestor of cartilaginous fishes, and that the OAS2 and the OAS3 genes evolved from a mammalian ancestor. OAS proteins function in the interferon system in mammals. This system is only found in jawed vertebrates. We therefore suggest that the original function of OAS may differ from its function in the interferon system, and that this original function of OAS is preserved even in OAS genes that code for proteins, which do not have 2′-5′-oligoadenylate synthetase activity.     

Scalable Fabrication of Efficient Perovskite Solar Modules on Flexible Glass Substrates

Perovskite materials are good candidates for flexible photovoltaic applications due to their strong absorption and low‐temperature processing, but efficient flexible perovskite modules have not yet been realized. Here, a record efficiency flexible perovskite solar module is demonstrated by blade coating high‐quality perovskite films on flexible Corning Willow Glass using additive engineering. Ammonium chloride (NH₄Cl) is added into the perovskite precursor solution to retard the nucleation which prevents voids formation at the interface of perovskite and glass. The addition of NH₄Cl also suppresses the formation of PbI₂ and reduces the trap density in the perovskite films. The implementation of NH₄Cl enables the fabrication of single junction flexible perovskite solar devices with an efficiency of 19.72% on small‐area cells and a record aperture efficiency of 15.86% on modules with an area of 42.9 cm². This work provides a simple way to scale up high‐efficiency flexible perovskite modules for various applications.