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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 Downloaded from www.microbiologyresearch.org by IP: 88.99.165.207 On: Thu, 15 Jun 2017 20:21:30 Printed in Great Britain 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 References Arisue, N., Sanchez, L. B., Weiss, L. M., Müller, M. & Hashimoto, T. (2002). Mitochondrial-type hsp70 genes of the amitochondriate protists, Giardia intestinalis, Entamoeba histolytica and two microsporidians. Parasitol Int 51, 9–16. Arisue, N., Hashimoto, T. & Yoshikawa, H. (2003). Sequence heterogeneity of the small subunit ribosomal RNA genes among Blastocystis isolates. Parasitology 126, 1–9. Bacchi, C. J., Rattendi, D., Faciane, E. & 7 other authors (2004). Polyamine metabolism in a member of the phylum Microspora (Encephalitozoon cuniculi): effects of polyamine analogues. Microbiology 150, 1215–1224. Hackstein, J. H., Akhmanova, A., Boxma, B., Harhangi, H. R. & Voncken, F. G. (1999). Hydrogenosomes: eukaryotic adaptations to anaerobic environments. Trends Microbiol 7, 441–447. Hashimoto, T., Sánchez, L. B., Shirakura, T., Müller, M. & Hasegawa, M. (1998). Secondary absence of mitochondria in Giardia lamblia and Trichomonas vaginalis revealed by valyl-tRNA synthetase phylogeny. Proc Natl Acad Sci U S A 95, 6860–6865. Karr, C. D. & Jarroll, E. L. (2004). Cyst wall synthase: N- acetylgalactosaminyltransferase activity is induced to form the novel N-acetylgalactosamine polysaccharide in the Giardia cyst wall. Microbiology 150, 1237–1243. Keithly, J. S., Zhu, G., Upton, S. J., Woods, K. M., Martinez, M. P. & Yarlett, N. (1997). Polyamine biosynthesis in Cryptosporidium parvum and its implications for chemotherapy. Mol Biochem Parasitol 88, 35–42. Knell, J. D., Allen, G. E. & Hazard, E. I. (1977). Light and electron microscope study of Thelohania solenopsae n. sp. (Microsporidia: Protozoa) in the red imported fire ant, Solenopsis invicta. J Invertebr Pathol 29, 192–200. Lantsman, Y., Tan, K. S. W. & Yarlett, N. (2003). Identification of a putative hydrogenosome-like organelle from Blastocystis hominis. In Proceedings of the VIII International Workshop on Opportunistic Protists and International Conference on Anaerobic Protists, Hilo, Hawaii, July 25–29. Abstract no. C10. León-Avila, G. & Tovar, J. (2004). Mitosomes of Entamoeba histo- lytica are abundant mitochondrion-related remnant organelles that lack a detectable organellar genome. Microbiology 150, 1245–1250. Lloyd, D. (2004). ‘Anaerobic protists’: some misconceptions and confusions. Microbiology 150, 1115–1116. Lloyd, D., Harris, J. C., Maroulis, S., Wadley, R., Ralphs, J. R., Hann, A. C., Turner, M. P. & Edwards, M. R. (2002). The ‘primitive’ microaerophile Giardia intestinalis (syn. lamblia, duodenalis) has specialized membranes with electron transport and membranepotential-generating functions. Microbiology 148, 1349–1354. Lloyd, D., Harris, J. C., Biagini, G. A., Hughes, M. R., Maroulis, S., Bernard, C., Wadley, R. B. & Edwards, M. R. (2004). The plasma membrane of microaerophilic protists: oxidative and nitrosative stress. Microbiology 150, 1183–1190. Mai, Z., Ghosh, S., Frisardi, M., Rosenthal, B., Rogers, R. & Samuelson, J. (1999). Hsp60 is targeted to a cryptic mitochondrion- derived organelle (‘‘crypton’’) in the microaerophilic protozoan parasite Entamoeba histolytica. Mol Cell Biol 19, 2198–2205. Millership, J. J., Cai, X. & Zhu, G. (2004a). Functional characteriza- tion of replication protein A2 (RPA2) from Cryptosporidium parvum. Microbiology 150, 1197–1205. Millership, J. J., Waghela, P., Cai, X., Cockerham, A. & Zhu, G. (2004b). Differential expression and interaction of transcription co- activator MBF1 with TATA-binding protein (TBP) in the apicomplexan Cryptosporidium parvum. Microbiology 150, 1207–1213. 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F. (2003). iron–sulphur protein maturation. Nature 426, 172–176. Ultrastructural characterization and further transmission studies of Thelohania solenopsae from Solenopsis invicta. J Invertebr Pathol 83, 177–180. Yoshikawa, H., Abe, N. & Wu, Z. (2004). PCR-based identification http://mic.sgmjournals.org of zoonotic isolates of Blastocystis from mammals and birds. Microbiology 150, 1147–1151. Downloaded from www.microbiologyresearch.org by IP: 88.99.165.207 On: Thu, 15 Jun 2017 20:21:30 1129