Download Anaerobic protists and hidden mitochondria

Microbiology (2004), 150, 1127–1129
Overview
DOI 10.1099/mic.0.27174-0
Anaerobic protists and hidden mitochondria
Nigel Yarlett
Correspondence
Nigel Yarlett
Department of Chemistry and Physical Sciences and Haskins Laboratories, Pace University,
New York, NY 10038, USA
[email protected]
Anaerobic protists special issue
This issue contains papers pertaining to the joint International Conference on Anaerobic Protists (ICAP) and VIII
International Workshop on Opportunistic Protists (IWOP),
held at Hilo, Hawaii, 25–29 July 2003. At first glance these
two broad categories might seem rather disparate; however,
upon closer inspection there is a common ground and that
is the organisms’ loosely categorized into these two camps
often lack mitochondria and have in several instances
mitochondrial remnant organelles. Linked to the lack of
recognizable mitochondria is the fact that many of the
representatives in these groups live under low-oxygen
conditions. In compiling this issue, we have concentrated
on bringing together a range of studies that aim to extend
the biochemical, molecular, physiological and taxonomic
knowledge of organisms that live under low-oxygen conditions. One of the challenges of modern science is to better
understand the relationship that exists between the variously
developed structures collectively described as mitochondrial
remnant organelles and the role of anaerobiosis in this
event. The current Comment article by Lloyd (2004) puts
into focus some of the misconceptions concerning anaerobiosis and, hence, I recommend readers of this issue to
note the importance of realizing that what is commonly
referred to as anaerobic is really an incorrect dogma. The
hydrogenosome once thought of as the anaerobic equivalent
of the mitochondria, with a separate evolutionary lineage,
has many similarities to mitochondria and is probably a
divergent organelle (Müller, 1993). I will deliberately avoid
the use of the word ‘archaic’ in this overview as this term
has been extensively used and abused in the literature to
describe organisms that had no identifiable mitochondria
or mitochondria-like structures. This view has changed
recently with the finding of mitochondrial remnant organelles termed mitosomes in Entamoeba (Mai et al., 1999;
Tovar et al., 1999): this coupled with the presence of
mitochondrial chaperonin genes (Arisue et al., 2002) confirms the secondary loss of mitochondria by this organism
and this has been reviewed by Müller (2000). The presence
of specialized membranes with electron transport functions has also been detected in Giardia (Lloyd et al., 2002).
This organism once considered amitochondriate has
mitochondrial-like chaperonin genes (Roger et al., 1998;
Arisue et al., 2002), a nuclear coded valyl-tRNA synthetase
(Hashimoto et al., 1998) and has recently been demonstrated
to contain a fully functional mitochondrial iron–sulphur
0002-7174 G 2004 SGM
cluster assembly pathway involving the proteins IscS and
IscU which are present in a double membrane-bound
mitochondrial remnant organelle (Tovar et al., 2003). However, with the exception of Nyctotherus ovalis (Hackstein
et al., 1999), all mitochondrial remnant organelles, including
hydrogenosomes, lack an organelle genome, which was the
major distinction between mitochondria and hydrogenosomes (Müller, 1993). The recently discovered Entamoeba
remnant mitochondrial organelle, the mitosome, also lacks
an organelle genome (León-Avila & Tovar, 2004), suggesting that reduction in organelle function was accompanied
by loss of the genome. It is clear from several studies that
these so-called anaerobes do encounter varying amounts
of oxygen and therefore must have the ability to survive
the effects of oxidative stress, and this is explored in
the report by Lloyd et al. (2004). A mitochondrial relict
organelle has also been described in cryptosporidia (Riordan
et al., 2003). This observation was recently supported by
the finding that Cryptosporidium parvum has genes (IscS
and IscU) encoding a mitochondrial-type iron–sulphur
cluster biosynthetic pathway and that these proteins target
the proposed relict organelle. Thus, C. parvum is the latest
to join the growing numbers that support the view that
there are no truly amitochondriate extant eukaryotes
(Müller, 2000). The report of mitochondrial-type hsp70
genes in two microsporidians strongly suggests that this
group of amitochondriates has also undergone secondary
mitochondrial loss (Arisue et al., 2002).
Polyamines are found in diverse cell types but the precise
mechanism of polyamine metabolism varies in different
species. Polyamine metabolism in the microsporidian
Encephalitozoon cuniculi was found to differ considerably
from other eukaryotes (Bacchi et al., 2004), where it is
believed to rely upon spermine uptake and back-conversion
to spermidine and putrescine. Polyamine biosynthesis by
C. parvum was also reported to differ considerably from
other eukaryotes, being more like that of plants and certain
bacteria (Keithly et al., 1997). Two reports dealing with
various molecular aspects of cryptosporidia are included
in this issue and examine the replication protein A2 (RPA2)
and the interaction of the transcription co-activator MBF1
with the TATA-binding protein (Millership et al., 2004a, b).
These reports illustrate the molecular advances that are
occurring in this area of research.
Many of the microaerophilic protists produce cysts that are
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1127
N. Yarlett
capable of surviving unfavourable conditions: included in
this group are Entamoeba, Cryptosporidium and Giardia.
The mechanism and biochemistry of cyst wall formation is
intrinsic to the survival and often the parasitism of the
protist. This process is clearly of great significance to the
development of potential chemotherapeutic agents. Giardia
has a cyst cell wall that is approximately 37 % protein and
63 % carbohydrate. The major carbohydrate of the cyst wall
is N-acetyl-D-galactosamine [D-GalNAc(b1-3)D-GalNAc]n.
The galactose N-acetyl polysaccharide cell-wall constituent
is unique to Giardia and is synthesized by six enzymes
starting with glucosamine-6-phosphate isomerase and
ending with N-acetylgalactosaminyltransferase that is
induced during encystment (Karr & Jarroll, 2004). During
this process oxygen uptake rates double from the nonencysting stage and this process is inhibited by metronidazole. In addition, amino sugar phosphate levels increase
during encystation (Sener et al., 2004). These findings are
of significance to future trends in the potential chemotherapy of this parasite.
The presence of multiple spore types in the microsporidian
Thelohania solenopsae has been described; these include the
unicellular meiospores (octospores), macrospores, megaspores and a diplokaryotic spore found exclusively in pupae
(Knell et al., 1977; Sokolova & Fuxa, 2001; Shapiro et al.,
2003). The PCR-amplified SSU rDNA nucleotide sequences
from these spores have been examined and compared by
use of position ablative laser microbeam microscopy
(Sokolova et al., 2004). The genotype of Blastocystis is
highly polymorphic and studies aimed at species identification have been hindered by lack of a suitable method to
distinguish human and animal parasites. The development
of several sequence-tagged site primers derived from
randomly amplified polymorphic DNA has been used to
identify genotypes that correspond to phylogenetically
different clades inferred from the small-subunit rRNA
genes (SSU rDNA) (Arisue et al., 2003; Yoshikawa et al.,
2004).
It is clear that the diversity of eukaryotic cells that have
undergone secondary loss of the mitochondrion is growing
and the preliminary description of a mitochondrial remnant
organelle in Blastocystis hominis (Lantsman et al., 2003)
extends this further. However, a cautionary note is needed
as the majority of anaerobic eukaryotes examined to date
have also undergone secondary adaptation to a parasitic or
symbiotic lifestyle within low-oxygen-containing cavities
of the host. The exploration of eukaryotes from potentially much older anaerobic environments, such as deepsea sediments and sulphide sediments, may yet reveal an
amitochondriate eukaryote.
It is clear from the scope and variety of presentations at
the joint ICAP IWOP meeting that research on anaerobic
protists has expanded; however, many questions concerning
the biochemical adaptations that have occurred amongst
this group remain to be answered.
1128
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