Journal of Applied Phycology (2006) 18: 475–481
DOI: 10.1007/s10811-006-9054-6
C Springer 2006
A genomic and phylogenetic perspective on endosymbiosis and algal origin
Hwan Su Yoon, Jeremiah D. Hackett & Debashish Bhattacharya∗
Department of Biological Sciences and Roy J. Carver Center for Comparative Genomics, University of Iowa, 446
Biology Building, Iowa City, Iowa 52242-1324
∗
Author for correspondence: e-mail: debashi-bhattacharya@uiowa.edu; fax: (319) 335-1069
Received 4 August 2004; accepted 17 November 2004
Key words: algal evolution, chromalveolates, endosymbiosis, gene transfer, plastid
Abstract
Accounting for the diversity of photosynthetic eukaryotes is an important challenge in microbial biology. It has
now become clear that endosymbiosis explains the origin of the photosynthetic organelle (plastid) in different algal
groups. The first plastid originated from a primary endosymbiosis, whereby a previously non-photosynthetic protist
engulfed and enslaved a cyanobacterium. This alga then gave rise to the red, green, and glaucophyte lineages.
Algae such as the chlorophyll c-containing chromists gained their plastid through secondary endosymbiosis, in
which an existing eukaryotic alga (in this case, a rhodophyte) was engulfed. Another chlorophyll c-containing
algal group, the dinoflagellates, is a member of the alveolates that is postulated to be sister to chromists. The
plastid in these algae has followed a radically different path of evolution. The peridinin-containing dinoflagellates
underwent an unprecedented level of plastid genome reduction with the ca. 16 remaining genes encoded on 1–3
gene minicircles. In this short review, we examine algal plastid diversity using phylogenetic and genomic methods
and show endosymbiosis to be a major force in algal evolution. In particular, we focus on the evolution of targeting
signals that facilitate the import of nuclear-encoded photosynthetic proteins into the plastid.
Introduction
The eukaryotic photosynthetic organelle (plastid) is
critical to life on our planet because of its contribution to global primary production. Ten different types
of plastids are known and are found in evolutionarily divergent eukaryotic clades (Baldaif et al., 2000;
Bhattacharya et al., 2004). The endosymbiosis hypothesis was put forth to explain the origin of plastids
and mitochondria (Margulis, 1970; Mereschkowsky,
1905) and has been extensively supported with modern molecular evolutionary analyses. In plastid primary
endosymbiosis, a non-photosynthetic protist engulfed
a cyanobacterium and converted it into a permanent
photosynthetic organelle. This photosynthetic eukaryote gave rise to the red, green, and glaucophyte algae
that have a plastid bound by two membranes. Thereafter, plastids were horizontally spread into the remaining photosynthetic protist groups through secondary
endosymbiosis, in which non-photosynthetic cells engulfed an existing (red or green) alga. This proces
resulted in the plastid of cryptophytes, haptophytes,
stramenopiles, apicomplexans, dinoflagellates (red
algal endosymbiont), euglenophytes, and chlorarachniophytes (green algal endosymbiont, Bhattacharya &
Medlin, 1995; Cavalier-Smith, 1986; Douglas, 1998;
Douglas et al., 1991; Gibbs, 1978; McFadden et al.,
1994; Yoon et al., 2002b; Zhang et al., 1999). However,
endosymbiosis did not stop there because in dinoflagellates the existing plastid of red algal origin was replaced
on multiple independent occasions with this organelle
from an alga containing a secondary plastid (a cryptophyte, haptophyte or stramenopile: tertiary endosymbiosis) or a primary plastid (a green alga) (Chesnick
et al., 1997; Hackett et al., 2003; Ishida & Green, 2002;
Tengs et al., 2000; Watanabe et al., 1990; Yoon et al.,
2002a).
The development of large scale sequencing and genomic approaches has greatly augmented our understanding of algal evolution. These methods have been
applied to generate complete genome or expressed sequence tag (EST) databases of model algae or protists
476
as well as to generate broadly sampled multi-gene phylogenies. In this paper, we discuss algal diversity from
the perspective of plastid endosymbiosis, and present
a brief summary of recent findings from genomic and
phylogenetic approaches. In addition, we examine the
leader sequences of nuclear-encoded plastid genes that
have resulted from intracellular gene transfer and that
make possible plastid targeting.
Endosymbiosis is an important driving force in
algal evolution
Primary endosymbiosis
Rhodophyta, Viridiplantae (green algae and land
plants), and Glauco(cysto)phyta contain plastids surrounded by a double membrane that very likely originated through a single primary endosymbiosis in
the common ancestor of these taxa (Bhattacharya &
Medlin, 1995; Delwiche et al., 1995; Gray, 1992;
McFadden, 2001; Moreira et al., 2000; Matsuzaki et al.,
2004; McFadden & van Dooren, 2004). Molecular
clock analysis using a concatenated data set of six
plastid genes and multi-fossil calibrations suggest that
the primary endosymbiosis occurred around 1.6 billion
years ago (Yoon et al., 2004). This estimate has been
independently confirmed by multi-protein analyses of
nuclear loci that suggest a date of 1.6–1.5 BY for
primary plastid origin (Hedges et al., 2004; Hackett
et al., 2006). Despite their ancient origin, the monophyly of Plantae is moderately supported by recent
molecular phylogenetic studies using nuclear and mitochondrial genes (Baldauf et al., 2000; Moreira et al.,
2000; Palmer, 2003; Rodriguez-Ezpeleta et al., 2005).
A broadly sampled tree of microbial eukaryotes is urgently needed to test the monophyly of Plantae (and
other groups – see below).
Secondary endosymbiosis
The putative lineage Chromista, which comprises the
cryptophytes, haptophytes, and stramenopiles, contain chlorophyll c in their 4-membrane bound plastid
(Cavalier-Smith, 1986). The chromist plastid is not located in the cytosol but rather within the rough endoplasmic reticulum (RER), which is connected to
the outermost membrane of the plastid and is referred to as the chloroplast endoplasmic reticulum
(CER). Secondary endosymbiosis, in which the nonphotosynthetic ancestor of chromists engulfed an existing red alga, explains plastid origin in this group
(Bhattacharya & Medlin, 1995; Douglas et al., 1991;
Fast et al., 2001; Gibbs, 1981; Harper & Keeling, 2003).
Evidence for this secondary endosymbiosis comes
from the cryptophytes that retain the remnant nucleus
of the red algal endosymbiont, the nucleomorph, between the two inner and two outer plastid membranes.
The haptophytes and stramenopiles have presumably
lost the nucleomorph after their divergence from the
cryptophytes. Our molecular clock analysis suggests a
minimum age of 1.3 BY for this secondary endosymbiotic event and around 1.2 BY for the divergence of
cryptophytes from the other chromists and 1 BA for
the split of haptophytes and stramenopiles (Yoon et al.,
2004).
Alveolates, which comprise the dinoflagellates, apicomplexans, and ciliates, are postulated to be sister to
the chromists (together, the chromalveolates; CavalierSmith, 1999 [see Fast et al., 2001; Harper & Keeling,
2003; Bhattacharya et al., 2004]). The chromalveolate common ancestor most likely contained a red algal secondary endosymbiont (Cavalier-Smith, 1999)
that was apparently lost in the ciliates. In the apicomplexans, such as the well-known human parasite
Plasmodium falciparum Welch, the remnant plastid
(called the apicoplast) genome was reduced to a 35 Kb
circle (Williamson et al., 1994). However, the phylogenetic history of apicoplasts remains unclear because of
the high divergence of the encoded sequences that usually results in long branch artifacts in trees (Funes et al.,
2002; Waller et al., 2003; Zhang et al., 1999, 2000).
An important data set that supports chromalveolate
monophyly is the presence of a unique glyceraldehyde3-phosphate dehydrogenase (GAPDH) gene replacement shared by these taxa (Fast et al., 2001; Harper &
Keeling, 2003). In addition, because the plastid genes
of dinoflagellates were re-organized into mini-circles
and most of the plastid genes were transferred to the
nucleus (followed by high sequence divergence rates
in many of these coding regions), it is difficult to accurately infer the phylogeny of dinoflagellate plastids (Bachvaroff et al., 2004; Hackett et al., 2004;
Zhang et al., 1999). To resolve this issue, we sequenced
five minicircle-encoded plastid proteins from a handful of peridinin dinoflagellates and from fucoxanthincontaining taxa. These latter taxa presumably gained
their plastid through a haptophyte tertiary endosymbisois (Ishida & Green, 2002; Tengs et al., 2000; Yoon
et al., 2005). In the resulting trees, the evolutionary
origin of the peridinin plastids remains unclear but
this clade is clearly positioned as a monophyletic lineage within the red algae with a weak sister group
477
relationship to the stramenopiles. This result is consistent with the chromalveolate hypothesis and potentially
explains the monophyletic origin of the plastid (and by
extension, the host cells; Cavalier-Smith, 1999; Fast
et al., 2001; Harper & Keeling, 2003). However, it is
critical to verify this hypothesis with a broad taxon
sampling and a multi-gene analysis of the host cells.
Euglenophytes and chlorarachniophytes acquired
their green algal plastid through independent secondary
endosymbioses (Archibald & Keeling, 2002; Baldauf,
2003; Bhattacharya et al., 2004; Palmer, 2003). However, if secondary plastid loss has occurred more frequently then we postulate, genomic analysis may be
the best, and perhaps only, approach to identify the
number of plastid endosymbioses that have occurred
during eukaryotic evolution. The finding of nuclearencoded genes of photosynthetic function in presently
aplastidial cells will, for example, allow us to more accurately map the ancestral plastid distribution on the
host tree.
Moestrup which gained its plastid through a green algal secondary endosymbiosis (Archibald et al., 2003).
EST analysis of this taxon showed numerous lateral
transfers of genes from streptophyte, stramenopile, red
algal, and bacterial sources. Furthermore, the whole
genome sequence from the apicomplexan parasite P.
falciparum reveals that 11% (581/5268 proteins) of
genes of plastid function are still maintained in the nucleus (Gardner et al., 2002). It is interesting that these
genes are absent from another apicomplexan, Cryptosporidium parvum Tyzzer, that apparently lacks an
apicoplast (Abrahamsen et al., 2004). Taken together,
genomic approaches are becoming ever more popular
and result in an unprecedented quantity and quality
of data that provide critical evolutionary information.
However, it is important to keep in mind that single sequenced taxa (model or otherwise) do not adequately
represent the evolutionary diversity of eukaryotes and
taxonomically broadly sampled genomics projects hold
the greatest promise for clarifying algal evolution.
Genomic approaches for clarifying algal evolution
Protein import system: Leader sequence
Genomic methods such as whole genome random shotgun and EST approaches have recently been used to
significantly improve our understanding of algal evolution. In one study Martin et al. (2002) found that ca.
18% of the nuclear genes in Arabidopsis thaliana (L.)
Heynh. (of both photosynthetic and non-photosynthetic
function) originated through intracellular gene transfer from the original cyanobacterial primary endosymbiont. This suggests that primary endosymbiosis resulted in massive lateral gene transfer from the endosymbiont to the nucleus and subsequently resulted
in the enrichment and potential re-organization of the
nuclear genome.
Three EST studies have thus far been done with
dinoflagellates (i.e., Alexandrium tamarense (Lebour.)
E. Balech, Amphidinium carterae Hulburth, and
Lingulodinium polyedrum (F. Stein) J. D. Dodge)) and
many others are underway. These studies have identified a massive transfer of plastid genes to the nucleus (Bachvaroff et al., 2004; Hackett et al., 2004)
and intriguingly some of these genes are of green
algal origin. This suggests that that there has either
been multiple lateral gene transfers from green algal
sources or, less parsimoniously, an as yet unsubstantiated green algal endosymbiosis (Hackett et al., 2004).
Other examples of gene transfer have been reported
in the chlorarachniophyte alga, Bigelowiella natans
Following transfer to the nucleus, the proper function
of the proteins involved in plastid function relies on
their successful import into this organelle. This process occurs because of the presence of a N-terminal
extension on each protein that specifies organellar import (Martin & Herrmann, 1998). The nature of these
“leader” sequences depends on the ultrastructure of the
plastid, such as the number of bounding membranes,
and the location of the organelle in the cytoplasm (for
detailed review, see Kilian & Kroth, 2003).
Two-membrane plastids located in the cytosol
The cyanobacterial origin of plastids bound by two
membranes is strongly supported by the finding of homology of the protein import channel of the translocon
of the inner/outer envelope of the plastid (i.e., Tic20,
Tic55, and Toc75) among plants and cyanobacteria
(Eckart et al., 2002; Heins et al., 1998; Kilian & Kroth,
2003). The green, red, and glaucophyte algae contain
leader sequences (Figure 1A) to target proteins to the
plastidial Tic/Toc system (see Matsuzaki et al., 2004;
McFadden & van Dooren, 2004). These residues are
encoded on the 5 -terminus of the open reading frame
and are of length 25–125 amino acids (Cavalier-Smith,
2000; McFadden, 1999; Nassoury et al., 2003; Waller
et al., 1998). Within the plastid, an endopeptidase
478
Figure 1. Plastid origin and the protein import system in photosynthetic eukaryotes. The protein import system reflects the plastid ultrastructure
rather than the source of the organelle. (A) After primary endosymbiosis, massive plastid gene transfer (GT) occurred to the nucleus (Nu). A
transit peptide (TP) that modified the N-terminus targets the functional proteins to the 2-membrane bound plastid (P) through the translocon of
the inner/outer plastid envelope (TIC/TOC). This import system is found in algae containing primary endosymbionts, however, it may also be
present in the 2-membrane bound plastid of the dinoflagellates Dinophysis and Lepidodinium. (B) Chromista that contain 4-membrane plastids
with a chloroplast endoplasmic reticulum (CER) have a modified bipartite leader sequence, which targets the proteins to the CER with the signal
peptide (SP) in addition to typical transit peptide. (C) The secretory pathway (ER and Golgi apparatus) is involved in the protein import system in
the apicomplexa and chlorarachniophytes. The small circle represents microsomes (m) that contain the transit peptide and the functional protein
via the secretory pathway. (D) The 3-membrane bound plastid in the dinoflagellates and euglenophytes contain a tripartite leader sequence. The
second hydrophobic region (ST) acts as a stop transfer signal that generates a functional protein in the cytoplasm (m). CB, cyanobacterium; CR,
cryptophyte; HA, haptophyte; RH, rhodophyte; VI, Viridiplantae.
cleaves the leader sequence (transit peptide). The twomembrane bound plastid in the dinoflagellates, Dinophysis spp. and Lepidodinium viride M. Watanabe, S.
Suda, I. Inoye, T. Sawaguchi and M. Chihara which did
not originate through primary endosymbiosis (rather
via cryptophyte and green algal plastid replacements,
respectively), most likely use the Tic import pathway
of the inner plastid membrane that has been found in
all algae and plants (McFadden & van Dooren, 2004).
Four-membrane bound plastids located in the CER of
the lumen
In addition to the two inner membranes, chromists contain an additional two membranes that necessitate a
more complex targeting signal (Figure 1B). Because
the plastid of chromists is located in the CER, targeting
into this membrane requires a classic signal peptide that
has a hydrophobic region (Apt et al., 2002). This bipartite leader sequence subsequently targets the protein
across the inner two membranes with a downstream
transit peptide.
Four-membrane plastids located in the cytosol
Although the plastids of apicomplexans and chlorarachniophytes are of independent origins (from a red
and a green alga, respectively), they both contain a
four-membrane bound plastid located in the cytosol
(unlike the chromists, Figure 1C). The bi-partite leader
sequence, that specifies a signal peptide and a transit peptide, target the proteins into the cytosolic RER
where the signal peptide is cleaved (McFadden, 1999;
479
Waller et al., 1998). During passage through the Golgi
system, the secretory vesicles fuse with the outermost
membrane of the plastid and thereafter, the transit peptide directs the protein through the Tic/Toc system. A
secretory system-dependent transport system has been
found in the four-membrane bound apicoplast in P.
falciparum and surprisingly, as well as in the threemembrane bound plastid in Euglena gracilis G. A.
Klebs and Gonyaulax polyedra F. Stein that do not contain a CER (Nassoury et al., 2003; Sulli et al., 1999;
Waller et al., 2000).
Three membrane-bound plastids located in the cytosol
Dinoflagellates and euglenophytes contain plastids
bound by three membranes that do not have a connection between the outer plastid membrane and the endomembranes (Figure 1D). Tripartite leader sequences,
which consist of a hydrophobic signal peptide, a transit
peptide, and a second hydrophobic region, were found
in these taxa (Hackett et al., 2004; Nassoury et al.,
2003; Sulli et al., 1999). The second hydrophobic region acts as a “stop transfer signal” and the functional
protein is located in the cytoplasmic side of the ER after
cleavage of the signal peptide (Nassoury et al., 2003).
Microsomes that contain the functional transit peptide pass through the membranes via a secretory pathway (Golgi apparatus) followed by subsequent vesicular transport across the cytoplasm before entering the
plastids (Nassoury et al., 2003; Sulli et al., 1999). A
tripartite leader sequence in the psbO gene has been
identified from the fucoxanthin-containing dinoflagellate, Karenia brevis (C. C. Davis) G. Hansen & Ø.
Moestrup (Ishida & Green, 2002).
springs (Lopez-Garcia et al., 2001; Moon-van der Staay
et al., 2001; Ciniglia et al., 2004). Furthermore, the
picoplankton in both coastal and open ocean environments promises to be a potentially endless source of
novel taxa. Because many of these lineages are positioned basal in trees, the environmental PCR method
provides a powerful tool for understanding early algal
evolution. In this regard, the finding that many basal
lineages such as the marine stramenopiles and alveolates are heterotrophic, forces us to postulate multiple
secondary plastid losses in chromalveolates to be consistent with the ideas presented here.
Recently, an environmental meta-genomic approach
using shotgun whole genome sequencing was used to
study bacterial diversity in the oligotrophic Sargasso
Sea (Venter et al., 2004). This breakthrough work
identified at least 1800 genomic species including
148 previously unknown bacterial phylotypes and over
1.2 million previously unknown genes. Although an
imprecise and incomplete approach to generating complete genome sequences, this remarkable body of data
challenges all biologists to account more rigorously
for microbial diversity when studying eukaryotic and
in particular, algal evolution. Clearly, we are just beginning to understand the complex history of microbial
eukaryotes and the future holds great promise in clarifying the phylogeny of algae and their place in the tree
of life.
Acknowledgements
This work was primarily supported by grants from
the United States National Science Foundation to D.B.
(grants DEB 01-07754, MCB 02-36631).
Conclusions
Great progress has recently been made in generating
the outline of the eukaryotic tree of life using molecular
phylogenies (e.g., Baldauf, 2003). The deep branches
of the tree remain however unsubstantiated and await a
rigorous multi-gene approach with a broad taxonomic
sampling. This type of analysis will ultimately resolve
the main splits in the algal tree and establish the timing of algal origins. The methods of phylogenetics and
genomics provide significant data but the challenge remains to extensively sample representatives of all the
major algal groups and relevant non-algal groups. Our
understanding of algal biodiversity has also been significantly changed by environmental PCR analyses of
extreme environments such as the deep sea and hot
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