The Physiology of Phagocytosis in the Context of Mitochondrial Origin - PubMed (original) (raw)
Review
The Physiology of Phagocytosis in the Context of Mitochondrial Origin
William F Martin et al. Microbiol Mol Biol Rev. 2017.
Abstract
How mitochondria came to reside within the cytosol of their host has been debated for 50 years. Though current data indicate that the last eukaryote common ancestor possessed mitochondria and was a complex cell, whether mitochondria or complexity came first in eukaryotic evolution is still discussed. In autogenous models (complexity first), the origin of phagocytosis poses the limiting step at eukaryote origin, with mitochondria coming late as an undigested growth substrate. In symbiosis-based models (mitochondria first), the host was an archaeon, and the origin of mitochondria was the limiting step at eukaryote origin, with mitochondria providing bacterial genes, ATP synthesis on internalized bioenergetic membranes, and mitochondrion-derived vesicles as the seed of the eukaryote endomembrane system. Metagenomic studies are uncovering new host-related archaeal lineages that are reported as complex or phagocytosing, although images of such cells are lacking. Here we review the physiology and components of phagocytosis in eukaryotes, critically inspecting the concept of a phagotrophic host. From ATP supply and demand, a mitochondrion-lacking phagotrophic archaeal fermenter would have to ingest about 34 times its body weight in prokaryotic prey to obtain enough ATP to support one cell division. It would lack chemiosmotic ATP synthesis at the plasma membrane, because phagocytosis and chemiosmosis in the same membrane are incompatible. It would have lived from amino acid fermentations, because prokaryotes are mainly protein. Its ATP yield would have been impaired relative to typical archaeal amino acid fermentations, which involve chemiosmosis. In contrast, phagocytosis would have had great physiological benefit for a mitochondrion-bearing cell.
Keywords: endocytic pathway; eukaryogenesis; eukaryote evolution; metagenomics; mitochondria; phagocytosis.
Copyright © 2017 American Society for Microbiology.
Figures
FIG 1
Mitochondrion-late and mitochondrion-early models for the origin of eukaryotes. Fossil evidence has it that eukaryotes are 1.5 billion to 1.8 billion years old (329, 330). All current models for the origin of eukaryotes have mitochondria in the eukaryote common ancestor. (A) In mitochondrion-late models, an archaeon (red) becomes a complex protoeukaryote, evolves phagocytosis, and acquires the proteobacterium (blue). The sequence of the emergence of compartments differs substantially across phagotrophic origin models: some have the nucleus first, and others have primitive phagocytosis or undefined endomembranes. Some mitochondrion-late models posit the participation of additional prokaryotic partners at eukaryote origin, for example, for the origin of the nucleus or the origin of the flagellum (26, 331). (B) In mitochondrion-early models, phagocytosis came after the mitochondrion. Mitochondrion-early models typically start with metabolic interactions between an archaeon and the proteobacterial ancestor of mitochondria (26). Models that entail anaerobic syntrophy to account for the origin of mitochondria simultaneously account for the common ancestry of mitochondria and hydrogenosomes (18, 90). In mitochondrion-early models, the origin of eukaryote-specific structures like the nucleus, the endomembrane system, and flagella, but also the origin of eukaryote-specific processes like phagocytosis, mitosis, meiosis, and sex (170), occurred after the phagocytosis-independent entry of the endosymbiont into the host's cytosol. In one formulation of mitochondrion-early models (199), outer membrane vesicles (OMVs) of the mitochondrial endosymbiont (mitochondrion-derived vesicles [MDVs]) physically gave rise to the first vesicles of the endomembrane system.
FIG 2
Bioenergetic membranes in phagocytosis and protein translocation. Eukaryogenesis models rarely consider the role and fate of bioenergetic membranes. (A) The vacuolar ATPase of eukaryotes is of archaeal origin, which suggests that the archaeal host synthesized ATP at its plasma membrane. This poses a problem concerning the phagocytic origin of mitochondria. A phagocytosing archaeon would digest its own ATP synthesis machinery, an energetically unfavorable condition. (B) Bioenergetic membranes are characterized by a proton motive force (PMF), here symbolized by plus and minus signs. The proton motive force influences protein secretion through the SecYEG and TAT machineries at the prokaryotic plasma membrane via electrophoretic properties but also in eukaryotes at the inner (bioenergetic) membrane of the mitochondrion (155, 332). Both prokaryotic signal peptides and targeting peptides of mitochondrial matrix proteins carry positively charged amino acid residues that respond to the proton motive force. Upon endosymbiosis, the presence of two independent bioenergetic membranes (and a proton motive force) likely would have fostered false targeting. Eukaryotic cells today have retained one bioenergetic membrane, the inner mitochondrial membrane, which also has retained the use of the proton motive force for protein translocation. Targeting to the eukaryotic plasma membrane commences with cotranslational import into the rough endoplasmic reticulum (rER) through the Sec61 translocon (which stems from archaeal SecYEG) that is targeted by eukaryotic signal peptides that have lost their positively charged character (in contrast to their prokaryotic signal peptides). TOM, translocase of the outer mitochondrial membrane; TIM, translocase of the inner mitochondrial membrane; TAT, twin arginine translocon.
FIG 3
Amino acids as a source of energy. Aerobic ATP yields (174) are shown on the left and correspond to the net ATP yield for the complete oxidation of the amino acids to carbon dioxide by mammals via the intermediates shown on the right. The end products of anaerobic amino acid breakdown pathways in eukaryotes have not been determined. The expected degradation pathways of amino acids to intermediates that can be broken down further to fermentation products by anaerobically functioning mitochondria to generate ATP are shown. Branched arrows are used to show that the degradation of one molecule of the amino acid in question results in the two products. The possible yields of ATP of these anaerobic pathways are discussed in the text.
FIG 4
Endocytic processes to scale. There are many separate endocytic processes that can occur at the eukaryotic plasma membrane. Among all eukaryotic supergroups, three main types are found: phagocytosis, clathrin-independent endocytosis (CIE), and clathrin-mediated endocytosis, while caveolae are restricted to metazoans and appear to have evolved later in evolution. All of these processes have in common that they require an elaborate set of proteins, downstream processing through the endomembrane system that includes the early endosome and multivesicular bodies (MVB), and recycling of certain protein components and membranes back to the plasma membrane through vesicles. The different processes are shown roughly to scale for comparison at the plasma membrane. Clathrin-independent endocytosis, caveolae, and clathrin-mediated endocytosis are also enlarged to highlight a few details, such as the absence or presence of a coat. Both phagocytosis and clathrin-mediated endocytosis depend on dynamin for terminal membrane scission. Dynamin is likely of mitochondrial origin and absent from archaeal genomes.
FIG 5
From prokaryotes to eukaryotes through endosymbiosis. Prokaryotic life belongs to either the bacterial or archaeal group. Prokaryotes are descended from the last universal common ancestor (LUCA) that marks the origin of life. Eukaryogenesis and the origin of the last eukaryotic common ancestor (LECA) hinge upon the endosymbiotic acquisition of a bacterial endosymbiont (the mitochondrion) by an archaeal host. The pivotal role of mitochondrial acquisition for the emergence of eukaryotes is evident through the existence of mitochondria in all eukaryotic supergroups (and, hence, the eukaryote common ancestor), among which no family that lacks mitochondria or mitochondrion-derived organelles is known. The Archaeplastida, uniting algae and plants, emerged after the endosymbiotic origin of the plastid from a cyanobacterium.
FIG 6
The in and out of vesicles. Vesicles form at both prokaryotic and eukaryotic plasma membranes. There are, however, crucial differences. Prokaryotic vesicles are secreted into the environment only through blebbing of the plasma membrane away from the cytosol. These types of vesicles are known as OMVs, and they are found among all types of prokaryotes. Archaeal OMVs are also released with the help of proteins of the CDV family (
c
ell
d
i
v
ision) that are homologous to eukaryotic ESCRT proteins. The topology in the function of the ESCRT (
e
ndosomal
s
orting
c
omplex
r
equired for
t
ransport) machinery in eukaryotes has been conserved, as the eukaryotic ESCRT machinery, like the archaeal CDV machinery, works on membranes that are bending away from the cytosol. Eukaryotic vesicles can be secreted into the environment (exosomes) or into the cytosol through endocytic mechanisms. Endocytic vesicle maturation often requires the formation of a complex coat that is usually composed of a combination of membrane proteins and peripheral proteins that interact with each other (Table 1). Endocytic mechanisms are receptor mediated, like, for example, in the case of iron uptake from the environment by the transferrin receptor that is internalized through the formation of clathrin-coated vesicles.
FIG 7
Prokaryotic partnerships: alternatives to phagocytosis. There are many examples of syntrophic interactions among prokaryotes and a few rare cases of one prokaryote residing within another. (A) Transmission electron micrographs of longitudinal sections of Pleurocapsa minor showing intracellular bacteria. (Reproduced from reference with permission of John Wiley and Sons.) (B) Infection of the Pseudomonas fluorescens periplasm by Bdellovibrio bacteriovorus. (Courtesy of Edouard Jurkevitch; reproduced with permission.) (C) Transmission electron micrograph showing nested, multilayer endosymbiosis inside the bacteriome of a mealybug (Pseudococcidae). Bacteriomes carry betaproteobacterial Trembleya endosymbionts, which themselves carry gammaproteobacterial Morganella endosymbionts. b, bacteria; n, nucleus; ss, symbiotic sphere. (Reproduced from reference by permission from Macmillan Publishers Ltd.) (D) Transmission electron micrograph of Parakaryon myojinensis harboring endosymbionts of an unknown nature (marked with “E”). NM, nuclear membrane; PM, plasma membrane; N, nucleus. (Reproduced from reference with permission [copyright the author 2012; published by Oxford University Press {on behalf of Japanese Society of Microscopy}].) (E) Confocal laser scanning micrograph of in situ hybridization of bacteria (green) and archaea (red). (Reproduced from reference by permission from Macmillan Publishers Ltd.) (F) Confocal images of consortia of bacteria (green) and archaea (orange). The picture on the right side is a false-color image that highlights the nitrogen-fixing properties of archaeal cells. (Reproduced from reference with permission from AAAS.) (G) Fluorescence in situ hybridization of HotSeep-1 bacteria (green) that receive reducing equivalents from their archaeal partner (red). (Reproduced from reference by permission from Macmillan Publishers Ltd.) (H) Stacks of electron-dense hydrogenosomes (darker) in the cytosol of the ciliate Plagiopyla frontata sandwiched between methanogens (lighter gray structures). (Reproduced from reference with permission of Springer.)
References
- Jorgensen SL, Hannisdal B, Lanzén A, Baumberger T, Flesland K, Fonseca R, Øvreås L, Steen IH, Thorseth IH, Pedersen RB, Schleper C. 2012. Correlating microbial community profiles with geochemical data in highly stratified sediments from the Arctic Mid-Ocean Ridge. Proc Natl Acad Sci U S A 109:E2846–E2855. doi:10.1073/pnas.1207574109. - DOI - PMC - PubMed
- Zaremba-Niedzwiedzka K, Caceres EF, Saw JH, Bäckström D, Juzokaite L, Vancaester E, Seitz KW, Anantharaman K, Starnawski P, Kjeldsen KU, Stott MB, Nunoura T, Banfield JF, Schramm A, Baker BJ, Spang A, Ettema TJG. 2017. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541:353–358. doi:10.1038/nature21031. - DOI - PubMed
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources