Mitochondria –Our Ancient Allies Get a New Sister Clade

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Mitochondria in lung tissue – Photo by Louisa Howard

Mitochondria are the quintessentially bacterial endosymbionts that call our cells home and, in return for food and shelter, produce most of our energy. But mitochondrial talents don’t end at energy production –they also metabolize amino acids (think proteins), lipids (fats) and iron as well as initiate and regulate programmed cell death (apoptosis). In fact, many scientists think mitochondria make most of the key decisions about whether a cell lives or dies, which diseases we get and how we age. So how did these little bacteria get so powerful and where did they come from?

Some bacteria learned to make oxygen and others to live with it

It’s mostly about free oxygen, which was almost certainly non-existent on early earth. Oxygen, which was chemically bound to other elements when it arrived here from distant stars, eventually found a perfect mate in hydrogen and formed water.

More water was delivered to Planet Earth via meteorites and possibly comets and about 200 million years after our planet was born it had liquid on its surface. Why is this important? Because life as we know it is dependent on water and the oxygen (O2) that can be made from it.

Photosynthesis: The overwhelming source of free oxygen on earth is generated from the photobiological oxidation of water –and this requires bacteria. Oxygen-generating bacteria arose once from a single clade, were engulfed by other cells to form new organisms and became the progenitors of all photosynthetic eukaryotes including algae and higher plants, say Paul G. Falkowski from Rutgers University in New Brunswick New Jersey and Yukio Isozaki from the University of Tokyo in Japan. Using the sun’s energy, the new photosynthesizing microbes flooded early earth with oxygen in the form of O2and that brings us back to mitochondria.

Aerobic respiration: While some bacteria were busily ‘polluting’ the anaerobic world with oxygen, others began to exploit the new gas by learning how to ‘breathe’ it. “It seems reasonable to assume that the systems for aerobic respiration evolved in oceanic surface water because oxygenation probably started there,” says Björn Brindefalk at the Evolutionary Biology Center (EBC) in Uppsala, Sweden. Thus, Brindefalk and his boss Siv G.E. Andersson at EBC began searching the largest marine metagenomic sequencing database currently available, the Global Ocean Sampling (GOS), for ancestral mitochondria; the GOS put more than 6 million genes from ocean surface waters at their disposal.

Newly discovered mitochondrial sister clade overturns popular beliefs

Early analyses suggested that present day mitochondria originated from an alphaproteobacterial endosymbiont sometime after the rise of oceanic and atmospheric oxygen levels, says Andersson. Additional investigation further aligned mitochondria with the Rickettsiales, an obligate intracellular clade with members that are well adapted to life within the cytosol of eukaryotes such as protozoa, she adds.

Until recently it was thought that one specific alphaproteobacterial group, SAR 11 −which is represented by Candidatus Pelegibacter ubique– was the closest free-relative of mitochondria and Rickettsiales.  However, these researchers designed a new taxon jack-knifing procedure to extract GOS sequences clustering in the vicinity of the mitochondrial clade and this helped them systematically search for sequences more closely related to those of mitochondria than any of the existing alphaproteobacterial reference species had allowed them to do.

The re-designed phylogenetic test of a large metagenomic database revealed evidence of a free-living oceanic alphaproteobacterial clade which proved more closely related to Rickettsiales and, by inference, the mitochondrial progenitor than Ca.Pelagibacter ubique.  The newly discovered  group of alphaproteobacterial sequences has been dubbed “OMAC” for “Ocean Mitochondrial Affiliate Clade.”

Notably, OMAC is represented by GOS sequences in relatively low abundance in contrast to SAR 11 whose numbers dominate the ocean surface waters.

The Earth is a watery place – Photo courtesy of NASA

Oxygen-rich ocean surface waters prime source of clues to mitochondrial ancestors

“Future research aimed at identifying the mitochondrial progenitor should make ocean surfaces waters a priority,” Andersson says. Moreover, she urges that “models of the origin and evolution of eukaryotic cells and their organelles need to be re-examined in light of the full genetic diversity being uncovered by metagenome sequence data.”

Commenting on this research, Jonathan Eisen at the University of California, Davis, emphasizes how “valuable it is to do targeted phylogenetic analysis of metagenomic data,” and asks for further information about the differentiation of OMAC sequences from those of ocean-dwelling eukaryotic mitochondria or other endosymbionts. Andersson replies that mitochondria were indeed present in the dataset but these clustered with known mitochondrial sequences rather than those of OMAC. “If OMAC sequences were mitochondrial, it would consist of the most divergent form of mitochondria ever observed,” she adds noting that right now only the DNA sequences of these cells are available and “can’t wait to see what OMAC really looks like.

Giardia: Image by Dr. Stan Erlandsen; Dr. Dennis Feely,Center for Disease Control

Note: Judging by their popularity, mitochondria increase fitness. However; two present-day protozoa,  Microsporidia and Giardia, seem to be doing just fine without them and some scientists think they resemble, and may even be descended from, the anaerobic ancestral eukaryotes that originally engulfed mitochondrial precursors. Others, Bindefalk included, disagree, saying these anaerobic eukaryotes “once harbored mitochondria and subsequently lost them. Several theories for the origin of eukaryotes posit that the protomitochondrions werre integral to the event; in other words, there were no eukaryotes before ‘mitos’ were incorporated.”

Mitochondria in action:

Resources:

Personal communications:

Siv Andersson, PhD

Björn Brindefalk, PhD

Jonathan Eisen, PhD.

Additional sources:

Brindefalk B., Ettema T.J.G., Viklund J. et al. A Phylometagenomic Exploration of Oceanic Alphaproteobacteria Reveals Mitochondrial Relatives Unrelated to the SAR11 Clade. (2011) in PLoS ONE; 6(9): e24457. Doi:10.1371/journal.pone.0024457.

Falkowski P.G. and Isozaki Y. The Story of O2. (2008) in Science; 322:540-542.

Viklund J., Ettema T.J.G., Andersson S.G.E. Independent Genome Reduction and Phylogenetic Reclassification of the Oceanic SAR11 Clade. (2011) in Mol Biol Evol; doi:10.1093/molbev/ms 203.

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