The Diversity of Mitochondrion-Related Organelles Amongst Eukaryotic Microbes

Barberà, Maria José; Ruiz‐Trillo, Iñaki; Leigh, Jessica W.; Hug, Laura; Roger, Andrew J.

doi:10.1007/978-3-540-38502-8_10

Cited by 22 publications

(36 citation statements)

References 142 publications

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“…(28)(29)(30) Gene concatenation and supertree approaches with tens of protein-coding genes were recently used to reconstruct the phylogeny of the mitochondria within the a-proteobacteria. (28,(30)(31)(32) The emerging conclusion from these studies is that among the currently defined a-proteobacterial orders, the Rickettsiales are the closest to the mitochondria, with the Rhodospirillales coming next. This by no means supposes that the mitochondrion evolved from a Rickettsia-like bacterium as both are the result of independent reductive evolutionary paths originating in free-living ancestors.…”

Section: Models For the Origin Of Eukaryotes: A Historical Perspectivementioning

confidence: 97%

Predation between prokaryotes and the origin of eukaryotes

Davidov

Jurkevitch

2009

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Accumulating data suggest that the eukaryotic cell originated from a merger of two prokaryotes, an archaeal host and a bacterial endosymbiont. However, since prokaryotes are unable to perform phagocytosis, the means by which the endosymbiont entered its host is an enigma. We suggest that a predatory or parasitic interaction between prokaryotes provides a reasonable explanation for this conundrum. According to the model presented here, the host in this interaction was an anaerobic archaeon with a periplasm-like space. The predator was a small (facultative) aerobic alpha-proteobacterium, which penetrated and replicated within the host periplasm, and later became the mitochondria. Plausible conditions under which this interaction took place and circumstances that may have led to the contemporary complex eukaryotic cell are discussed.

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Section: Models For the Origin Of Eukaryotes: A Historical Perspectivementioning

confidence: 97%

Predation between prokaryotes and the origin of eukaryotes

Davidov

Jurkevitch

2009

BioEssays

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“…The potential functional diversity of MROs could even be greater since there are a myriad of additional poorly studied anaerobic protists that, in transmission electron microscopy studies (26), have been shown to contain MROlike structures that have yet to be intensively investigated. By studying their organelles, we can obtain important insights into their evolutionary origin, the range of their biochemical flexibility within the eukaryotic tree of life, and possibly even the origin of eukaryotes themselves (5).…”

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Sawyeria marylandensis (Heterolobosea) Has a Hydrogenosome with Novel Metabolic Properties

et al. 2010

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Protists that live under low-oxygen conditions often lack conventional mitochondria and instead possess mitochondrion-related organelles (MROs) with distinct biochemical functions. Studies of mostly parasitic organisms have suggested that these organelles could be classified into two general types: hydrogenosomes and mitosomes. Hydrogenosomes, found in parabasalids, anaerobic chytrid fungi, and ciliates, metabolize pyruvate anaerobically to generate ATP, acetate, CO 2 , and hydrogen gas, employing enzymes not typically associated with mitochondria. Mitosomes that have been studied have no apparent role in energy metabolism. Recent investigations of free-living anaerobic protists have revealed a diversity of MROs with a wider array of metabolic properties that defy a simple functional classification. Here we describe an expressed sequence tag (EST) survey and ultrastructural investigation of the anaerobic heteroloboseid amoeba Sawyeria marylandensis aimed at understanding the properties of its MROs. This organism expresses typical anaerobic energy metabolic enzymes, such as pyruvate:ferredoxin oxidoreductase, [FeFe]-hydrogenase, and associated hydrogenase maturases with apparent organelle-targeting peptides, indicating that its MRO likely functions as a hydrogenosome. We also identified 38 genes encoding canonical mitochondrial proteins in S. marylandensis, many of which possess putative targeting peptides and are phylogenetically related to putative mitochondrial proteins of its heteroloboseid relative Naegleria gruberi. Several of these proteins, such as a branched-chain alpha keto acid dehydrogenase, likely function in pathways that have not been previously associated with the well-studied hydrogenosomes of parabasalids. Finally, morphological reconstructions based on transmission electron microscopy indicate that the S. marylandensis MROs form novel cup-like structures within the cells. Overall, these data suggest that Sawyeria marylandensis possesses a hydrogenosome of mitochondrial origin with a novel combination of biochemical and structural properties.It is now widely accepted that the most recent common ancestor of extant eukaryotes possessed an endosymbiont-derived mitochondrial organelle of alphaproteobacterial ancestry (see reference 16 for a recent review). Although most wellknown eukaryotes contain mitochondria that aerobically respire to produce ATP, a vast diversity of anaerobic eukaryotic lineages have been discovered that lack classical mitochondrial structures. Instead of mitochondria, biochemically diverse double-membrane-bounded organelles have been found that function under low-oxygen conditions (for recent reviews, see references 5, 6, 17, 23, 54, and 57). The discovery and recent investigations of the functions of these mitochondrion-related organelles (MROs) has greatly expanded our understanding of both the conservation and diversity of functions that these organelles can perform.A number of protist lineages, including the parabasalids, several anaerobic ciliate groups, and anaerobic chy...

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“…Unlike most of their euglenozoan relatives (for example, kinetoplastids and euglenids), C. aureus lacks recognizable mitochondria with cristae, and instead possesses superficially arranged double-membrane bound organelles nearly identical in morphology to the well-described hydrogenosomes found in flagellates from other anoxic environments . Hydrogenosomes function to produce molecular hydrogen, acetate, CO 2 and adenosine-5 0 -triphosphate in anoxic environments (Barbera et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Identity of epibiotic bacteria on symbiontid euglenozoans in O2-depleted marine sediments: evidence for symbiont and host co-evolution

et al. 2010

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A distinct subgroup of euglenozoans, referred to as the 'Symbiontida,' has been described from oxygen-depleted and sulfidic marine environments. By definition, all members of this group carry epibionts that are intimately associated with underlying mitochondrion-derived organelles beneath the surface of the hosts. We have used molecular phylogenetic and ultrastructural evidence to identify the rod-shaped epibionts of the two members of this group, Calkinsia aureus and B.bacati, hand-picked from the sediments of two separate oxygen-depleted, sulfidic environments. We identify their epibionts as closely related sulfur or sulfide-oxidizing members of the epsilon proteobacteria. The epsilon proteobacteria generally have a significant role in deep-sea habitats as primary colonizers, primary producers and/or in symbiotic associations. The epibionts likely fulfill a role in detoxifying the immediate surrounding environment for these two different hosts. The nearly identical rod-shaped epibionts on these two symbiontid hosts provides evidence for a co-evolutionary history between these two sets of partners. This hypothesis is supported by congruent tree topologies inferred from 18S and 16S rDNA from the hosts and bacterial epibionts, respectively. The eukaryotic hosts likely serve as a motile substrate that delivers the epibionts to the ideal locations with respect to the oxic/anoxic interface, whereby their growth rates can be maximized, perhaps also allowing the host to cultivate a food source. Because symbiontid isolates and additional small subunit rDNA gene sequences from this clade have now been recovered from many locations worldwide, the Symbiontida are likely more widespread and diverse than presently known.

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The Diversity of Mitochondrion-Related Organelles Amongst Eukaryotic Microbes

Cited by 22 publications

References 142 publications

Predation between prokaryotes and the origin of eukaryotes

Predation between prokaryotes and the origin of eukaryotes

Sawyeria marylandensis (Heterolobosea) Has a Hydrogenosome with Novel Metabolic Properties

Identity of epibiotic bacteria on symbiontid euglenozoans in O2-depleted marine sediments: evidence for symbiont and host co-evolution

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