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Chlamydiae As Symbionts in Eukaryotes 115 ANRV354-MI62-07 ARI 5 August 2008 17:25 ANRV354-MI62-07 ARI 5 August 2008 17:25 ANNUAL REVIEWS Further Chlamydiae as Symbionts Click here for quick links to Annual Reviews content online, including: in Eukaryotes • Other articles in this volume • Top cited articles • Top downloaded articles Matthias Horn • Our comprehensive search Department of Microbial Ecology, University of Vienna, A-1090 Vienna, Austria; email: [email protected] by Universidade Federal do Parana on 03/04/10. For personal use only. Annu. Rev. Microbiol. 2008.62:113-131. Downloaded from arjournals.annualreviews.org Annu. Rev. Microbiol. 2008. 62:113–31 Key Words First published online as a Review in Advance on chlamydia, symbiosis, amoeba, evolution May 12, 2008 The Annual Review of Microbiology is online at Abstract micro.annualreviews.org Members of the phylum Chlamydiae are obligate intracellular bacteria This article’s doi: that were discovered about a century ago. Although Chlamydiae are ma- 10.1146/annurev.micro.62.081307.162818 jor pathogens of humans and animals, they were long recognized only Copyright c 2008 by Annual Reviews. as a phylogenetically well-separated, small group of closely related mi- All rights reserved croorganisms. The diversity of chlamydiae, their host range, and their 0066-4227/08/1013-0113$20.00 occurrence in the environment had been largely underestimated. To- day, several chlamydia-like bacteria have been described as symbionts of free-living amoebae and other eukaryotic hosts. Some of these envi- ronmental chlamydiae might also be of medical relevance for humans. Their analysis has contributed to a broader understanding of chlamy- dial biology and to novel insights into the evolution of these unique microorganisms. 113 ANRV354-MI62-07 ARI 5 August 2008 17:25 considered responsible for trachoma, which Contents was at that time a global disease (47). Within Giemsa-stained conjunctival epithelial cells of INTRODUCTION .................. 114 trachoma patients they had found irregularly DIVERSITY AND ECOLOGY OF blue-stained inclusions with small, dense par- CHLAMYDIA-LIKE ticles, which they called “Chlamydozoa” (from BACTERIA ....................... 115 the Greek word χλαμυσ, meaning mantle or Symbionts of Free-Living cloak) (47). Originally considered neither pro- Amoebae ....................... 116 tozoa nor bacteria and then regarded as viruses, Other Nonhuman Hosts ........... 117 in the 1960s they were recognized as bacteria The Tip of the Iceberg ............. 117 (84). Later, these unique microorganisms were CHLAMYDIA-LIKE BACTERIA: found to be among the most important bacterial IMPLICATIONS FOR pathogens of humankind. PUBLIC HEALTH?............... 119 Halberstadter’s¨ and Prowazek’s Chlamydo- The Case of Parachlamydia zoa are now called Chlamydia trachomatis, and it acanthamoebae ................... 120 is the most prominent representative of a small The Case of Simkania negevensis .... 120 group of closely related bacteria, the chlamy- Causal Relationships? .............. 120 diae. Trachomaaffects about 84 million people, Infections of Animals............... 121 of whom about 8 million are visually impaired BIOLOGY OF CHLAMYDIA-LIKE as a consequence (103). is also BACTERIA ....................... 121 C. trachomatis the most common cause of sexually transmitted Developmental Cycle .............. 121 diseases, with over 90 million new cases each Metabolism........................ 122 year (102). The second prime human pathogen Host Cell Interaction .............. 123 among the chlamydiae is EVOLUTIONARY HISTORY Chlamydophila pneumo- niae, a causative agent of pneumonia, which has OF THE CHLAMYDIAE .......... 124 also been associated with a number of chronic A Last Common Intracellular diseases such as atherosclerosis, asthma, and Ancestor........................ 124 Alzheimer’s disease (67). In addition, several by Universidade Federal do Parana on 03/04/10. For personal use only. Chlamydiae and the Origin other chlamydial species are primarily consid- of Plants........................ 124 ered pathogens of animals, but some of them The Closest Free-Living Relatives . 125 Annu. Rev. Microbiol. 2008.62:113-131. Downloaded from arjournals.annualreviews.org also show zoonotic potential (67). PERSPECTIVES .................... 125 Chlamydiae were long considered to com- prise exclusively obligate intracellular bacterial pathogens that show a characteristic develop- INTRODUCTION mental cycle, including metabolically inert el- ementary bodies (EBs) and actively dividing It has to be tried to collect by the term ‘Chlamy- reticulate bodies (RBs), which thrive within a dozoa’ a group of peculiar microorganisms that do host-derived vacuole termed inclusion (1). This belong neither to the protozoa nor to the bacteria. phylogenetically well-isolated group of closely They pass filters, cause inclusion bodies and will related bacteria constituted the single family multiply as contagium only in egg culture. Chlamydiaceae of the order Chlamydiales, which Stanislaus von Prowazek, 1912 (58) form a separate phylum in the domain Bacte- In Java, Indonesia, in 1907, the German radi- ria, the Chlamydiae (Figure 1). Our perception ologist Ludwig Halberstadter¨ and the Austrian of chlamydial diversity changed substantially zoologist Stanislaus von Prowazek went on a when in the 1990s novel chlamydia-like bacteria EB: elementary body research expedition to find the causative agent were discovered. This review summarizes our RB: reticulate body of syphilis. Among the discoveries they brought current knowledge about these novel chlamy- back from this trip was a conspicuous agent they diae (also called environmental chlamydiae). 114 Horn ANRV354-MI62-07 ARI 5 August 2008 17:25 Piscichlamydiaceae “ “Candidatus C Clavochlamydiaceae andidatu Chlamydiaceae Simkaniaceae ” Rhabdochlamydiaceae s 2 Rhabdochl Rhab Waddliaceae occi” A4 isiae Act 7 Criblamydiaceae oc m V doch lla U Parachlamydiaceae ivated be r OEW1 is s coc. Biofilm clone 44aB134 lamydia porc ea be e 0.01 amydia crassificans tu Chlamydoph chea eri ba sludge clone P17 Hall’ Chlamydophila abortu s nsis oe eno itsch Ch r Frit Ch X F lamydophi f rophila oebae s tham l o s am laysiensis m u Chlam tu diment clone LD1P y nt Chl d ellioni acan da op ila caviae io a sequane b a di ydia acanthamoebae h y negevens kania lia ma a my n ila dophi la psittaci 302 ym andidat dd d p s” mydia ophil UWE25 ophi Ca ddlia chond S a “ Sim C n ” lamydi Candi “ a eu “ Marine se Chlamydi la f W lone 5 gleri C la p W lamydia acantha UWE1 datus hla m s achla Chlamydia trac on e Crib r ch Clavoc my ecorum lis Parachlam a nea asp. ia soil c a m d Pa ara ydi hlam ia e P uridarum suis Parachlamydia acanthamoebaenthamoeb ydi Amazon Acti a sal homatis hlamydia Aca amoebophilane P4 orvenA4 vated Protochlamtoc t of ge clo lone c Freshwat slud monicola” Pro d slud lavage c e ge Symbion ar r clone clone vate velo 3 Freshwat LT100PI P6 Acti lone P “Candidatus er clone c H9 Bronchoal ludge c e Piscichlamydi ctivated s hartmannella vE6 A amydia 1 a salmonis” Neochl TUME Acanthamoeba sp. Symbiont of Figure 1 Phylogenetic 16S rRNA tree showing relationships among members of the phylum Chlamydiae. Representatives of all recognized families and a few clone sequences are shown. The tree was calculated with the ARB software, using a manually curated version of the SILVA database (16S/18S reference database, Version 92) and the PhyML treeing algorithm implemented in ARB, and visualized using the iTOL tool (43, 74, 77, 88). Bar, 10% estimated evolutionary distance. DIVERSITY AND ECOLOGY OF by Universidade Federal do Parana on 03/04/10. For personal use only. CHLAMYDIA-LIKE BACTERIA Number of families 250 8 Number of sequences Ultrastructural evidence of the presence Number of sequence Annu. Rev. Microbiol. 2008.62:113-131. Downloaded from arjournals.annualreviews.org of unidentified bacteria resembling known s 200 chlamydiae was available in the 1980s (92). Yet it 6 took another decade until the first chlamydia- 150 like bacteria were identified on the molecular 4 level, initially in laboratory cell culture (66) but 100 mainly as symbionts of free-living amoebae (2, Number of familie 5, 31, 54) [in this review the terms symbiosis 2 s and symbiont are used sensu deBary, i.e., to 50 include mutualism, parasitism, and commen- salism (19)]. These findings were the begin- 0 0 1992 1994 1996 1998 2000 2002 2004 2006 2008 ning of a series of reports describing a continu- Year ing increase of recognized diversity within the Figure 2 Chlamydiae (Figure 2) (16). Remarkably, these bacteria are not mere phylogenetic relatives of Increase in described diversity of the phylum Chlamydiae from 1992 to 2007. Numbers of 16S rRNA sequences deposited in public databases (>1000 the Chlamydiaceae; they also show an obligate nucleotides) and numbers of chlamydial families based on described chlamydiae intracellular lifestyle and the unique chlamydial [using the 90% 16S rRNA sequence similarity threshold suggested by Everett developmental cycle (Figure 3). et al. (25) and Kuo et al. (73)] are shown. www.annualreviews.org • Chlamydiae as Symbionts in Eukaryotes 115 ANRV354-MI62-07 ARI 5 August 2008 17:25 RB B D EB CB C A E G F by Universidade Federal do Parana on 03/04/10. For personal use only. Figure 3 The developmental cycle of chlamydia-like bacteria in free-living amoebae. Elementary bodies (EBs) are shown in blue; reticulate Annu. Rev. Microbiol. 2008.62:113-131. Downloaded from arjournals.annualreviews.org bodies (RBs) are in red, the proposed crescent bodies (CBs) of Parachlamydia acanthamoebae
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