Origins of eukaryotic cells – membrane lipids

The cell membrane is a fundamental and defining feature of cells.  The realization that the 3 domains of life: Bacteria, Archaea and Eukarya, have distinct membrane lipid compositions poses challenges and offers hints to reconstructing the evolutionary history of life on Earth.

The origin of eukaryotic cells is deeply puzzling, because even a superficial comparison of eukaryotic cells with prokaryotic cells reveals many complex innovations that seemingly arose all at once.  However, new and recent discoveries have revealed possible origins for some of these eukaryotic features in some groups of prokaryotes.

Shortly after the discovery and characterization of Archaea as an entirely new domain of life, separate from Bacteria and Eukarya, molecular phylogeny based on ribosomal RNA suggested that Archaea and Eukarya have a more recent common ancestor than Archaea and Bacteria, or Eukarya and Bacteria.  Indeed, Archaea and Eukarya have many genetic similarities. RNA polymerase, histone-like proteins, DNA polymerase are a few key examples (see review by Allers and Mevarech, 2005). However, many other genes in eukaryotes appear to be more similar to their bacterial homologues than to the Archaeal versions. The presence of both Archaeal and Bacterial genes in eukaryotic genomes have led to a number of hypotheses postulating various mash-ups between Bacteria and Archaea as a key originating event for eukaryotic evolution, with most favoring Archaea as a source of nuclear processes and Bacteria for cytoplasmic and metabolic processes (Cotton and McInerney, 2010).

Archaeal taxonomy, from Allers and Mevarech, Nature Reviews Genetics 6: 58-73

Some recent papers have focused attention on membrane lipids and membrane processes. Archaea have utterly different membrane lipid composition, with isoprenoid chains instead of fatty acids, L-glycerol instead of D-glycerol, and ether linkages instead of ester linkages (see http://www.ucmp.berkeley.edu/archaea/archaeamm.html and http://en.wikipedia.org/wiki/Archaea). Bacteria and Eukarya both have the familiar membrane phospholipids with esterified fatty acyl chains.

Ether-linked phospholipids in Archaea, compared with ester-linked phospholipids. Image from http://www.ucmp.berkeley.edu/archaea/archaeamm.html

Any hypothesis about the origin of eukaryotic cells must reconcile the archaeal characteristics of the eukaryotic information processing genes, against the absence of Archaeal characteristics from the eukaryotic membrane.

Eukaryotes also have membrane innovations that are not found in either Archaea or Bacteria: sterols and sphingolipids.  Sterols (like cholesterol) and sphingolipids are important components of eukaryotic plasma membranes, and together can constitute 50% of the lipids of the outer leaflet (Desmond and Gribaldo, 2009; sphingolipids are not found in the cytoplasmic side of the plasma membrane lipid bilayer).  Sterols are essential components of all eukaryotic cell membranes.  They modulate membrane fluidity and permeability.  Together with sphingolipids they help organize regions of the membrane into lipid rafts, microdomains in the plasma membrane with reduced fluidity, that organize cell signaling proteins into functional complexes (see review by Lingwood and Simons, 2010).

Sterol biosynthesis is a complex pathway that requires molecular oxygen (11 molecules of oxygen are required to synthesize just one molecule of cholesterol) (Desmond and Gribaldo, 2009).  Therefore, steroid biosynthesis could not have evolved before the Great Oxygenation Event, circa 2.4-2.5 billion years ago.  Significantly, this time coincides with the origin of eukaryotes.  Evolution of steroid biosynthesis pathways thus looks like one of the keys to evolution of eukaryotes.

A recent phylogenomic analysis (Desmond and Gribaldo 2009) inferred that the last eukaryotic common ancestor had a suite of enzymes for synthesis of a diverse array of sterols.  Intriguingly, a few bacterial lineages also synthesize sterols, and their genomes contain homologs of the genes for key sterol biosynthesis enzymes.  The question is whether:

1) these bacteria acquired these genes from eukaryotes, via lateral gene transfer (also called horizontal gene transfer), or

2) these genes are cousins to the eukaryotic sterol synthesis genes, descendants of genes present in a common ancestor of these bacteria and eukaryotes, or

3) these genes evolved independently in these bacteria, and similarities to eukaryotic genes arose by convergent evolution.

The last possibility seems quite implausible, given that there are multiple genes. Indeed the phylogenetic trees are consistent with two of the genes for the first steps in sterol biosynthesis sorting into distinct bacterial and eukaryotic lineages (see Desmond and Gribaldo, Fig. 6, shown below).

Desmond and Gribaldo 2009 Fig. 6. Erg1 genes from bacteria form a distanct group from the eukaryotic Erg1 genes

These results are consistent with either hypothesis 2) above, or lateral gene transfer very early in eukaryotic evolution.  Other bacterial sterol synthesis genes such as Erg7 clearly appear to have been acquired more than once from eukaryotes via lateral gene transfer, because these gene sequences appear in clusters with eukaryotic Erg7 gene sequences (Desmond and Gribaldo 2009 Fig. 8).

Desmond and Gribaldo 2009 Fig. 8. Erg7 in bacteria appears in a cluster with eukaryotic Erg7 genes

Do these findings then suggest that the eukaryotic cell membrane is descended or borrowed from Bacteria? Was the eukaryotic ancestor a bacterium that captured an Archaeon, with the Archaeon subsequently evolving into the nucleus? If, instead, an Archaeon was host to bacteria that became mitochondria, why would the cell membrane become bacterial instead of retaining Archaeal lipids? Time, and analyses of a greater diversity of genomes, may tell.

Works cited:

Allers, T, M Mevarech 2005. Archaeal genetics – the third way, Nature Reviews Genetics 6: 58-73 doi:10.1038/nrg1504

Cotton, JA, JO McInerney 2010. Eukaryotic genes of archaebacterial origin are more important than the more numerous eubacterial genes, irrespective of function, Proc. Natl. Acad Sci. USA published online before print doi: 10.1073/pnas.1000265107

Desmond, E, S Gribaldo 2009. Phylogenomics of sterol synthesis: insights into the origin, evolution, and diversity of a key eukaryotic feature, Genome Biol Evol 1: 364-381 doi: 10.1093/gbe/evp036

Lingwood, D, K Simons 2010. Lipid rafts as a membrane-organizing principle, Science 327: 46-50

Lonhienne, TGA, E Sagulenko, RI Webb, K-C Lee, J Franke, DP Devos, A Nouwens, BJ Carroll, JA Fuerst 2010. Endocytosis-like protein uptake in the bacterium Gemmata obscuriglobus, Proc. Natl. Acad Sci. USA published online before print doi: 10.1073/pnas.1001085107

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About jchoigt

I'm an Associate Professor in the School of Biology at Georgia Tech, and Faculty Coordinator of the Professional MS Bioinformatics degree program.
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