Organelle Genomes--Going, Going, Gone

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Science  07 Feb 1997:
Vol. 275, Issue 5301, pp. 790
DOI: 10.1126/science.275.5301.790

An organism without a genome? Inconceivable, at least for free-living creatures. But what about an obligate, long-term endosymbiont—such as the mitochondrion and chloroplast—“living” within another organism? These organelles have persisted within eukaryotic cells for a long time—about 1 to 2 billion years—and have lost or passed to the nucleus most of their genes. Yet all chloroplasts and respiring mitochondria retain a functional genome of at least five genes.

Now, however, a eukaryotic organelle—the hydrogenosome—has been identified as endosymbiotic in origin, yet it lacks a genome and is entirely dependent on the nucleus for its genetic livelihood (1).

The hydrogenosome occurs widely, but its history has been elucidated clearly only in trichomonads—largely parasitic, flagellated protists. These air-tolerating anaerobes lack classical mitochondria (and also peroxisomes) and instead possess unusual energy-generating hydrogenosomes (2). Recent studies from four groups show that the hydrogenosome of Trichomonas vaginalis is actually a highly derived mitochondrion (36). Like mitochondria, trichomonad hydrogenosomes have a double-membrane envelope, divide autonomously by fission, import proteins posttranslationally, and produce ATP by substrate-level phosphorylation (2, 7). However, they differ from mitochondria in that they lack a genome, cytochromes, the tricarboxylic acid cycle, and oxidative phosphorylation; they use enzymes (pyruvate:ferredoxin oxidoreductase and hydrogenase) typically restricted to anaerobes; and they produce large quantities of hydrogen.

Two main hypotheses have been advanced for the origin of the trichomonad hydrogenosome: It is either the product of an independent endosymbiosis of an anaerobic eubacterium (8) or a highly modified mitochondrion adapted to an anaerobic lifestyle (9). The latter hypothesis is now strongly supported by the demonstration that the Trichomonas nucleus carries genes for one (46) or all three (3) of the mitochondrial heat-shock proteins Hsp10, Hsp60, and Hsp70. [HN3] These Hsps are among the most reliable tracers of the eubacterial ancestry of both the mitochondrion and chloroplast, and all three Trichomonas Hsps ally firmly with mitochondrial Hsps in phylogenetic analyses (36). Immunological studies (3, 10) verify that the Hsp60 and Hsp70 proteins reside in the Trichomonas hydrogenosome. Although other interpretations cannot be ruled out (5), these data indicate a common origin for the mitochondrion and hydrogenosome; most likely, the hydrogenosome is a highly derived mitochondrion (36).

Hydrogenosomes are a spectacular example of the repeated evolution of biochemically similar organelles, as adaptations to life with little or no oxygen. Hydrogenosomes are present not only in trichomonads, but in a wide variety of otherwise unrelated anaerobic or microaerobic eukaryotes, virtually all of which lack “mitochondria.” These include several phylogenetically disparate lineages of ciliates (11), both free-living and rumen-dwelling; certain rumen fungi; and some percolozoan protists (2, 7). The hunt will now be on to find molecular phylogenetic clues to the ancestry of these independently derived hydrogenosomes. Ultrastructural affinities to mitochondria are observed only for hydrogenosomes of free-living ciliates (12), and hydrogenosomes of the rumen fungus Neocallimastix are claimed to be of either mitochondrial or peroxisomal origin (13).

These findings should also prompt renewed inquiry into the early evolution of the eukaryotic cell and of eukaryotic phylogeny in general. The prevailing view for the past 10 years has been that the mitochondrion is not an ancestral feature of the eukaryotic cell (14, 15). This follows from ribosomal RNA (rRNA) phylogenies, which generally place three amitochondrial groups—trichomonads, microsporidians, and diplomonads—at the base of the eukaryotic tree (15). [HN4] But it is now clear that trichomonads do contain “mitochondria” (36). There is increasing evidence that microsporidians are misplaced in rRNA trees and are actually highly derived fungi that have lost mitochondria and most other organelles in the course of becoming obligate intracellular parasites (16); and there is suggestive immunological evidence (as yet unconfirmed by gene isolation) that diplomonads may also contain an Hsp60 of mitochondrial origin (17). These considerations led to the proposition (6) that the common ancestor of all extant eukaryotes contained mitochondria (and peroxisomes) and was thus aerobic, and that subsequent evolution has been reductive, not acquisitive (with the exception of the chloroplast).

One endeavor these findings should not stimulate is a renewed search for a genome in hydrogenosomes. All characterized mitochondrial genomes are geared solely toward the hallmark function of the organelle—respiration (18). Since loss of respiration is a defining feature of hydrogenosomes, one would also expect rapid loss of their mitochondrial genome, making such a search pointless. In contrast, plastid gene products, although geared largely toward photosynthesis—the hallmark function of the chloroplast—are involved in other important metabolic processes as well. Consequently, a residual, functional plastid genome persists in the plants, algae, and other protists that have lost photosynthesis (19) (see figure).

Origins of organelles.

The secondary chloroplast shown still contains a residual nucleus; other secondary chloroplasts have lost their nuclei [see text and (22)].

Why organelle genomes at all? The present notion is that plastids and respiring mitochondria have kept their genomes because some of the key integral membrane proteins of respiration and photosynthesis are intensely hydrophobic and are therefore unimportable across the organellar outer membranes (20). Mitochondrial genome retention may ultimately be driven by the only two proteins (both highly hydrophobic) encoded by all examined mitochondrial genomes (18, 20), whereas photosynthetic plastids encode about 10 times as many putatively unimportable proteins (20, 21). Unfortunately, this theory fails to account for genome retention in three disparate lineages of nonphotosynthetic plastids, which do not encode any hydrophobic proteins (19). Nor does it explain the surprising diversity of organelle genomes in both number and kind of gene products (18, 21).

Genomic extinction has also happened repeatedly for the nucleus in many cases of secondary plastid endosymbiosis, the process whereby a protist engulfs a eukaryotic alga and permanently retains part of its prey as a degenerate endosymbiont (22). In chlorarchniophytes and cryptomonads, a remnant of the algal endosymbiont's nucleus, termed the nucleomorph (and bearing a tiny genome of 380 to 660 kilobases), persists between the inner and outer pair of membranes surrounding its chloroplast (see figure). But in all other cases, the endosymbiotic nucleus (or nucleomorph) has vanished (22). This means that hundreds of ancestrally plastid genes must have been transferred twice during evolution, first from the plastid to the nucleus (then nucleomorph) after primary plastid endosymbiosis, and then again from the nucleomorph to the host nucleus after each of many independent secondary symbioses. All in all, then, the host nucleus seems to be a tremendous magnet, both for organellar genes and for endosymbiotic nuclear genes.

HyperNotes Related Resources on the World Wide Web

The Dictionary of Cell Biology (Second edition), edited by J.M. Lackie and J.A.T. Dow (London: Academic Press, 1995) defines many of the terms used in this article:

Endosymbiont hypothesis







TCA (tricarboxylic acid) cycle

The Glossary of Microbiology, compiled by Tsute Chen, defines endosymbiont.

The MIT Biology Hypertextbook, developed by the Experimental Study Group at the Massachusetts Institute of Technology, provides background information on the biology of cells and organelles. Structure and Function of Organelles, a section within Cell Biology, provides descriptions, diagrams, and photomicrographs for the most common organelles of plant and animal cells. Central Dogma describes the synthesis of proteins based on templates contained in the genome. Prokaryotic Genetics and Gene Expression explains gene expression in prokaryotes.

Mitochondria: Structure-Function Correlations describes the mitochondrion and includes diagrams and photomicrographs.

MITOMAP, human mitochondrial genome database developed at Emory University, provides functional maps and other information on the human mitochondrial genome.

A photomicrograph of the mitochondrion is included in the WWW Cell Biology Course.

C. elegans Mitochondrial Genome provides a map of the genome of the Chaenorhabditis elegans mitochondrial genome and descriptions of genes.

Organellar Genome Databases, a page maintained by the UK HGMP Resource Centre, provides links to information on mitochondrial and other organellar genomes. The page includes links to the Organelle Genome Megasequencing Program and the Organelle Genome Database at the University of Montreal.

The Virtual Cell is an interactive view of the cell developed at the University of Illinois. It includes illustrations and basic information about organelles.

Evolution of Eukaryotes, a lecture developed at the Department of Biological Sciences at the University of Alberta, presents the theories of eukaryotic evolution and explains the endosymbiotic theory.

The Gaia Hypothesis includes a discussion of the work of Lynn Margulis on the endosymbiotic theory.

The World Wide Web Virtual Library: Evolution (Biology) provides a long list of World Wide Web resources in evolution. The World Wide Web Virtual Library: Biochemistry and Molecular Biology (Biosciences) covers resources in molecular biology, biochemistry, and cell biology.

CSUBIOWEB, the California State University Biological Sciences Web server, provides links to other Web sites on cell biology and evolution.

1. Jeffrey D. Palmer

2. Department of Biology, Indiana University

3. McKay Lab Research Interests describes the work of Dave McKay and his co-workers and includes a description of the heat-shock protein HSP70.

4. The Tree of Life shows relationships between amitochondrial and mitochondrial eukaryotes.

5. Nucleomorph Chromosome III (from the article by P. Gilson, G.I. McFadden).

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