Mitochondria are membrane-bound components within cells that are often described as the cells' powerhouses. They've long been considered as essential components for life in eukaryotes, the group including plants, fungi, animals, and unicellular protists, if for no other reason than that every known eukaryote had them. But researchers reporting in the Cell Press journal Current Biology on May 12, 2016 now challenge this notion. They've discovered a eukaryote that contains absolutely no trace of mitochondria at all.
"In low-oxygen environments, eukaryotes often possess a reduced form of the mitochondrion, but it was believed that some of the mitochondrial functions are so essential that these organelles are indispensable for their life," says Anna Karnkowska, a former post-doctoral fellow at Charles University in Prague who is now at the University of British Columbia in Vancouver, Canada. "We have characterized a eukaryotic microbe which indeed possesses no mitochondrion at all."
Organisms from the genus Monocercomonoides have been recognized for more than 80 years. They are related to the human pathogens Giardia and Trichomonas, all of which belong to a group known as Metamonada, which lives exclusively in low-oxygen environments.
In the new study, Karnkowska and Vladimir Hampl at Charles University in Prague and BIOCEV, along with colleagues from the Czech Republic and Canada, sequenced the Monocercomonoides genome. They were surprised to find that this organism lacks all mitochondrial proteins.
Late acquisition of mitochondria by a host with chimaeric prokaryotic ancestry
Authors:
Pittis et al
Abstract:
The origin of eukaryotes stands as a major conundrum in biology1. Current evidence indicates that the last eukaryotic common ancestor already possessed many eukaryotic hallmarks, including a complex subcellular organization1, 2, 3. In addition, the lack of evolutionary intermediates challenges the elucidation of the relative order of emergence of eukaryotic traits. Mitochondria are ubiquitous organelles derived from an alphaproteobacterial endosymbiont4. Different hypotheses disagree on whether mitochondria were acquired early or late during eukaryogenesis5. Similarly, the nature and complexity of the receiving host are debated, with models ranging from a simple prokaryotic host to an already complex proto-eukaryote1, 3, 6, 7. Most competing scenarios can be roughly grouped into either mito-early, which consider the driving force of eukaryogenesis to be mitochondrial endosymbiosis into a simple host, or mito-late, which postulate that a significant complexity predated mitochondrial endosymbiosis3. Here we provide evidence for late mitochondrial endosymbiosis. We use phylogenomics to directly test whether proto-mitochondrial proteins were acquired earlier or later than other proteins of the last eukaryotic common ancestor. We find that last eukaryotic common ancestor protein families of alphaproteobacterial ancestry and of mitochondrial localization show the shortest phylogenetic distances to their closest prokaryotic relatives, compared with proteins of different prokaryotic origin or cellular localization. Altogether, our results shed new light on a long-standing question and provide compelling support for the late acquisition of mitochondria into a host that already had a proteome of chimaeric phylogenetic origin. We argue that mitochondrial endosymbiosis was one of the ultimate steps in eukaryogenesis and that it provided the definitive selective advantage to mitochondria-bearing eukaryotes over less complex forms.
Pleistocene Mitochondrial Genomes Suggest a Single Major Dispersal of Non-Africans and a Late Glacial Population Turnover in Europe
Authors:
Posth et al
Abstract:
How modern humans dispersed into Eurasia and Australasia, including the number of separate expansions and their timings, is highly debated [ 1, 2 ]. Two categories of models are proposed for the dispersal of non-Africans: (1) single dispersal, i.e., a single major diffusion of modern humans across Eurasia and Australasia [ 3–5 ]; and (2) multiple dispersal, i.e., additional earlier population expansions that may have contributed to the genetic diversity of some present-day humans outside of Africa [ 6–9 ]. Many variants of these models focus largely on Asia and Australasia, neglecting human dispersal into Europe, thus explaining only a subset of the entire colonization process outside of Africa [ 3–5, 8, 9 ]. The genetic diversity of the first modern humans who spread into Europe during the Late Pleistocene and the impact of subsequent climatic events on their demography are largely unknown. Here we analyze 55 complete human mitochondrial genomes (mtDNAs) of hunter-gatherers spanning ∼35,000 years of European prehistory. We unexpectedly find mtDNA lineage M in individuals prior to the Last Glacial Maximum (LGM). This lineage is absent in contemporary Europeans, although it is found at high frequency in modern Asians, Australasians, and Native Americans. Dating the most recent common ancestor of each of the modern non-African mtDNA clades reveals their single, late, and rapid dispersal less than 55,000 years ago. Demographic modeling not only indicates an LGM genetic bottleneck, but also provides surprising evidence of a major population turnover in Europe around 14,500 years ago during the Late Glacial, a period of climatic instability at the end of the Pleistocene.
Nuclear and mitochondrial DNA sequences from two Denisovan individuals
Authors:
Sawyer et al
Abstract:
Denisovans, a sister group of Neandertals, have been described on the basis of a nuclear genome sequence from a finger phalanx (Denisova 3) found in Denisova Cave in the Altai Mountains. The only other Denisovan specimen described to date is a molar (Denisova 4) found at the same site. This tooth carries a mtDNA sequence similar to that of Denisova 3. Here we present nuclear DNA sequences from Denisova 4 and a morphological description, as well as mitochondrial and nuclear DNA sequence data, from another molar (Denisova 8) found in Denisova Cave in 2010. This new molar is similar to Denisova 4 in being very large and lacking traits typical of Neandertals and modern humans. Nuclear DNA sequences from the two molars form a clade with Denisova 3. The mtDNA of Denisova 8 is more diverged and has accumulated fewer substitutions than the mtDNAs of the other two specimens, suggesting Denisovans were present in the region over an extended period. The nuclear DNA sequence diversity among the three Denisovans is comparable to that among six Neandertals, but lower than that among present-day humans.
pop sci write up at Nat Geo.
Two contemporaneous mitogenomes from terminal Pleistocene burials in eastern Beringia
Authors:
Tackney et al
Abstract:
Pleistocene residential sites with multiple contemporaneous human burials are extremely rare in the Americas. We report mitochondrial genomic variation in the first multiple mitochondrial genomes from a single prehistoric population: two infant burials (USR1 and USR2) from a common interment at the Upward Sun River Site in central Alaska dating to ∼11,500 cal B.P. Using a targeted capture method and next-generation sequencing, we determined that the USR1 infant possessed variants that define mitochondrial lineage C1b, whereas the USR2 genome falls at the root of lineage B2, allowing us to refine younger coalescence age estimates for these two clades. C1b and B2 are rare to absent in modern populations of northern North America. Documentation of these lineages at this location in the Late Pleistocene provides evidence for the extent of mitochondrial diversity in early Beringian populations, which supports the expectations of the Beringian Standstill Model.
pop sci write up.
Ancient Homology of the Mitochondrial Contact Site and Cristae Organizing System Points to an Endosymbiotic Origin of Mitochondrial Cristae
Authors:
Muñoz-Gómez et al
Abstract:
Mitochondria are eukaryotic organelles that originated from an endosymbiotic α-proteobacterium. As an adaptation to maximize ATP production through oxidative phosphorylation, mitochondria contain inner membrane invaginations called cristae. Recent work has characterized a multi-protein complex in yeast and animal mitochondria called MICOS (mitochondrial contact site and cristae organizing system), responsible for the determination and maintenance of cristae [ 1–4 ]. However, the origin and evolution of these characteristic mitochondrial features remain obscure. We therefore conducted a comprehensive search for MICOS components across the major groups that encompass eukaryotic diversity to determine the extent of conservation of this complex. We detected homologs for the majority of MICOS components among opisthokonts (the group containing animals and fungi), but only Mic60 and Mic10 were consistently identified outside this group. The conservation of Mic60 and Mic10 in eukaryotes is consistent with their central role in MICOS function [ 5–7 ], indicating that the basic mechanism for cristae determination arose early in evolution and has remained relatively unchanged. We found that eukaryotes with ultrastructurally simplified anaerobic mitochondria that lack cristae have also lost MICOS. We then searched for a prokaryotic MICOS and identified a homolog of Mic60 present only in α-proteobacteria, providing evidence for the endosymbiotic origin of mitochondrial cristae. Our study clarifies the origins of mitochondrial cristae and their subsequent evolutionary history, provides evidence for a general mechanism of cristae formation and maintenance in eukaryotes, and points to a new potential factor involved in membrane differentiation in prokaryotes.
Ancient dynamin segments capture early stages of host–mitochondrial integration
Authors:
Purkanti et al
Abstract:
Eukaryotic cells use dynamins—mechano-chemical GTPases—to drive the division of endosymbiotic organelles. Here we probe early steps of mitochondrial and chloroplast endosymbiosis by tracing the evolution of dynamins. We develop a parsimony-based phylogenetic method for protein sequence reconstruction, with deep time resolution. Using this, we demonstrate that dynamins diversify through the punctuated transformation of sequence segments on the scale of secondary-structural elements. We find examples of segments that have remained essentially unchanged from the 1.8-billion-y-old last eukaryotic common ancestor to the present day. Stitching these together, we reconstruct three ancestral dynamins: The first is nearly identical to the ubiquitous mitochondrial division dynamins of extant eukaryotes, the second is partially preserved in the myxovirus-resistance-like dynamins of metazoans, and the third gives rise to the cytokinetic dynamins of amoebozoans and plants and to chloroplast division dynamins. The reconstructed sequences, combined with evolutionary models and published functional data, suggest that the ancestral mitochondrial division dynamin also mediated vesicle scission. This bifunctional protein duplicated into specialized mitochondrial and vesicle variants at least three independent times—in alveolates, green algae, and the ancestor of fungi and metazoans—accompanied by the loss of the ancient prokaryotic mitochondrial division protein FtsZ. Remarkably, many extant species that retain FtsZ also retain the predicted ancestral bifunctional dynamin. The mitochondrial division apparatus of such organisms, including amoebozoans, red algae, and stramenopiles, seems preserved in a near-primordial form.
Phylogenomic Reconstruction Indicates Mitochondrial Ancestor Was an Energy Parasite
Authors:
Wang et al
Abstract:
Reconstruction of mitochondrial ancestor has great impact on our understanding of the origin of mitochondria. Previous studies have largely focused on reconstructing the last common ancestor of all contemporary mitochondria (proto-mitochondria), but not on the more informative pre-mitochondria (the last common ancestor of mitochondria and their alphaproteobacterial sister clade). Using a phylogenomic approach and leveraging on the increased taxonomic sampling of alphaproteobacterial and eukaryotic genomes, we reconstructed the metabolisms of both proto-mitochondria and pre-mitochondria. Our reconstruction depicts a more streamlined proto-mitochondrion than these predicted by previous studies, and revealed several novel insights into the mitochondria-derived eukaryotic metabolisms including the lipid metabolism. Most strikingly, pre-mitochondrion was predicted to possess a plastid/parasite type of ATP/ADP translocase that imports ATP from the host, which posits pre-mitochondrion as an energy parasite that directly contrasts with the current role of mitochondria as the cell’s energy producer. In addition, pre-mitochondrion was predicted to encode a large number of flagellar genes and several cytochrome oxidases functioning under low oxygen level, strongly supporting the previous finding that the mitochondrial ancestor was likely motile and capable of oxidative phosphorylation under microoxic condition.
