Membranes and evolution Gould, Sven B.
CB/Current biology,
04/2018, Volume:
28, Issue:
8
Journal Article
Peer reviewed
Open access
Biological membranes are thin amphiphilic sheaths, only a few nanometres thick, that define both the boundaries of all cells as well as the diversity of the internal compartments in eukaryotes. The ...plasma membrane of a typical prokaryote houses about 20–30% of the cell’s expressed proteins, and its lipids account for approximately 10% of the cell’s dry mass. The numbers for eukaryotic cells are comparable — the difference in surface area to volume ratio is overall compensated by the eukaryotic endomembrane system. Roughly a fourth of the protein encoded by the human genome carries at least one stretch of sequence predicted to serve as a transmembrane domain. Membranes host substrate exchange, sensing and communication, and life-giving energy conservation via chemiosmotic ATP synthesis.
Biological membranes are as varied as the life forms that produce them. Sven Gould takes a look at the evolution of membranes, from the last universal common ancestor, to the highly specialized membranes of complex organelles.
Highlights • Endosymbiotic theory explains why organelles resemble free-living bacteria. • Gene trees are well-suited to testing endosymbiotic theory, but not to replacing it. • Testing endosymbiotic ...theory requires that we keep LGT and pangenomes in mind. • The SELMA translocon is an important marker to trace secondary endosymbioses. • The lack of intermediates between prokaryotes and eukaryotes has a bioenergetic cause.
Streptophytes are unique among photosynthetic eukaryotes in having conquered land. As the ancestors of land plants, streptophyte algae are hypothesized to have possessed exaptations to the ...environmental stressors encountered during the transition to terrestrial life. Many of these stressors, including high irradiance and drought, are linked to plastid biology. We have investigated global gene expression patterns across all six major streptophyte algal lineages, analyzing a total of around 46,000 genes assembled from a little more than 1.64 billion sequence reads from six organisms under three growth conditions. Our results show that streptophyte algae respond to cold and high light stress via expression of hallmark genes used by land plants (embryophytes) during stress–response signaling and downstream responses. Among the strongest differentially regulated genes were those associated with plastid biology. We observed that among streptophyte algae, those most closely related to land plants, especially Zygnema, invest the largest fraction of their transcriptional budget in plastid-targeted proteins and possess an array of land plant-type plastid-nucleus communication genes. Streptophyte algae more closely related to land plants also appear most similar to land plants in their capacity to respond to plastid stressors. Support for this notion comes from the detection of a canonical abscisic acid receptor of the PYRABACTIN RESISTANCE (PYR/PYL/RCAR) family in Zygnema, the first found outside the land plant lineage. We conclude that a fine-tuned response toward terrestrial plastid stressors was among the exaptations that allowed streptophytes to colonize the terrestrial habitat on a global scale.
Eukaryotes possess an elaborate endomembrane system with endoplasmic reticulum, nucleus, Golgi, lysosomes , peroxisomes , autophagosomes , and dynamic vesicle traffic. Theories addressing the ...evolutionary origin of eukaryotic endomembranes have overlooked the outer membrane vesicles (OMVs) that bacteria, archaea, and mitochondria secrete into their surroundings. We propose that the eukaryotic endomembrane system originated from bacterial OMVs released by the mitochondrial ancestor within the cytosol of its archaeal host at eukaryote origin. Confined within the host's cytosol, OMVs accumulated naturally, fusing either with each other or with the host's plasma membrane. This matched the host's archaeal secretory pathway for cotranslational protein insertion with outward bound mitochondrial-derived vesicles consisting of bacterial lipids , forging a primordial, secretory endoplasmic reticulum as the cornerstone of the eukaryotic endomembrane system. Video Abstract
The number and nature of endosymbioses involving red algal endosymbionts are debated. Gene phylogenies have become the most popular tool to untangle this issue, but they deliver conflicting results. ...As gene and lineage sampling has increased, so have both the number of conflicting trees and the number of suggestions in the literature for multiple tertiary, and even quaternary, symbioses that might reconcile the tree conflicts. Independent lines of evidence that can address the issue are needed. Here we summarize the mechanism and machinery of protein import into complex red plastids. The process involves protein translocation machinery, known as SELMA, that arose once in evolution, that facilitates protein import across the second outermost of the four plastid membranes, and that is always targeted specifically to that membrane, regardless of where it is encoded today. It is widely accepted that the unity of protein import across the two membranes of primary plastids is strong evidence for their single cyanobacterial origin. Similarly, the unity of SELMA-dependent protein import across the second outermost plastid membrane constitutes strong evidence for the existence of a single red secondary endosymbiotic event at the common origin of all red complex plastids. We furthermore propose that the two outer membranes of red complex plastids are derived from host endoplasmic reticulum in the initial red secondary endosymbiotic event.
Recent work has provided a mechanistic view of protein import into complex red plastids. The process involves a protein translocation machinery, known as SELMA.
Two eukaryotic compartments are of endosymbiotic origin, the mitochondrion and plastid. These organelles need to import hundreds of proteins from the cytosol. The import machineries of both are of ...independent origin, but function in a similar fashion and recognize N-terminal targeting sequences that also share similarities. Targeting, however, is generally specific, even though plastid targeting evolved in the presence of established mitochondrial targeting. Here we review current advances on protein import into mitochondria and plastids from diverse eukaryotic lineages and highlight the impact of charged amino acids in targeting. Their presence or absence alone can determine localization, and comparisons across diverse eukaryotes, and their different types of mitochondria and plastids, uncover unexplored avenues of protein import research.
Plastids in plants and algae evolved from the endosymbiotic integration of a cyanobacterium by a heterotrophic eukaryote. New plastids can only emerge through fission; thus, the synchronization of ...bacterial division with the cell cycle of the eukaryotic host was vital to the origin of phototrophic eukaryotes. Most of the sampled algae house a single plastid per cell and basal-branching relatives of polyplastidic lineages are all monoplastidic, as are some non-vascular plants during certain stages of their life cycle. In this Review, we discuss recent advances in our understanding of the molecular components necessary for plastid division, including those of the peptidoglycan wall (of which remnants were recently identified in moss), in a wide range of phototrophic eukaryotes. Our comparison of the phenotype of 131 species harbouring plastids of either primary or secondary origin uncovers that one prerequisite for an algae or plant to house multiple plastids per nucleus appears to be the loss of the bacterial genes
and
from the plastid genome. The presence of a single plastid whose division is coupled to host cytokinesis was a prerequisite of plastid emergence. An escape from such a monoplastidic bottleneck succeeded rarely and appears to be coupled to the evolution of additional layers of control over plastid division and a complex morphology. The existence of a quality control checkpoint of plastid transmission remains to be demonstrated and is tied to understanding the monoplastidic bottleneck.
Key steps in evolution are often singularities. The emergence of land plants is one such case and it is not immediately apparent why. A recent analysis found that the zygnematophycean algae represent ...the closest relative to embryophytes. Intriguingly, many exaptations thought essential to conquer land are common among various streptophytes, but zygnematophycean algae share with land plants the transfer of a few plastid genes to the nucleus. Considering the contribution of the chloroplast to terrestrialization highlights potentially novel exaptations that currently remain unexplored. We discuss how the streptophyte chloroplast evolved into what we refer to as the embryoplast, and argue this was as important for terrestrialization by freshwater algae as the host cell-associated exaptations that are usually focused upon.
Interest in better understanding plant terrestrialization is growing, and there has been a longstanding debate regarding the nature of the single common algal ancestor of land plants. Emerging sequence data has now uncovered zygnematophycean algae as the closest relatives.
These data are also uncovering a growing list of exaptations among fresh-water (streptophyte) algae that are thought to be beneficial for conquering soil. Among them are factors often selected for in crop plants, such as the ability to cope with abiotic stress factors (e.g., high light stress) or the ability to engage in symbiotic relationships with fungi that aid in nutrient uptake.
None of these factors are, however, restricted to a single group of streptophyte algae, and the enigmatic question remains why terrestrialization was a single monophyletic event.
Plastid evolution Gould, Sven B; Waller, Ross F; McFadden, Geoffrey I
Annual review of plant biology,
01/2008, Volume:
59
Journal Article
Peer reviewed
The ancestors of modern cyanobacteria invented O(2)-generating photosynthesis some 3.6 billion years ago. The conversion of water and CO(2) into energy-rich sugars and O(2) slowly transformed the ...planet, eventually creating the biosphere as we know it today. Eukaryotes didn't invent photosynthesis; they co-opted it from prokaryotes by engulfing and stably integrating a photoautotrophic prokaryote in a process known as primary endosymbiosis. After approximately a billion of years of coevolution, the eukaryotic host and its endosymbiont have achieved an extraordinary level of integration and have spawned a bewildering array of primary producers that now underpin life on land and in the water. No partnership has been more important to life on earth. Secondary endosymbioses have created additional autotrophic eukaryotic lineages that include key organisms in the marine environment. Some of these organisms have subsequently reverted to heterotrophic lifestyles, becoming significant pathogens, microscopic predators, and consumers. We review the origins, integration, and functions of the different plastid types with special emphasis on their biochemical abilities, transfer of genes to the host, and the back supply of proteins to the endosymbiont.
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