Abstract
Many anaerobic ciliates possess hydrogenosomes, and consequently, they have the potential to host endosymbiotic methanogens. The endosymbiotic methanogens are vertically transmitted, and even cyst stages carry methanogens. Accordingly, the analysis of the SSU rRNA genes of ciliates and their methanogenic endosymbionts revealed that the endosymbionts are specific for their hosts and not identical with free-living methanogens. Notably, the endosymbionts of a monophyletic group of ciliates that thrive in either freshwater environments or intestinal tracts are substantially different. Ciliates from freshwater sediments host methanogens belonging to the Methanomicrobiales, while ciliates thriving in the intestinal tracts of cockroaches, millipedes and frogs host methanogens that belong to the Methanobacteriales. Comparative analysis of free-living and gut-dwelling ciliates and their corresponding endosymbionts reveals only a limited co-evolution suggesting infrequent endosymbionts replacements. Such an endosymbiont replacement is clearly the reason for the very distant endosymbionts of free-living and gut-dwelling ciliates: the endosymbionts are related to the methanogens in the particular environments, in which the hosts live.
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References
Adachi J, Hasegawa M (1996) MOLPHY Version 2.3. Programs for molecular phylogenetics based on maximum likelihood. Computer Science Monographs, no. 28. Institute of Statistical Mathematics, Tokyo, Japan
Bandi C, Damiani G, Magrassi L, Grigolo A, Fani R, Sacch L (1994) Flavobacteria as intracellular symbionts in cockroaches. Proc R Soc Lond B Biol Sci 257:42–48
Bandi C, Sironi M, Nalepa CA, Corona S, Sacchi L (1997) Phylogenetic distant intracellular symbionts in termites. Parasitologia 39:71–75
Baumann P, Lai C-Y, Baumann L, Rouhbakhsh D, Moran NA, Clark MA (1995) Mutualistic associations of aphids and prokaryotes: biology of the genus Buchnera. Appl Environ Microbiol 61:1–7
Baumann P, Moran NA, Baumann L (1997) The evolution and genetics of aphid endosymbionts. Bioscience 47:12–20
Boxma B, de Graaf RM, van der Staay GWM, van Alen TA, Ricard G, Gabaldon T, van Hoek AHAM, Moon-van der Staay SY, Koopman WJH, van Hellemond JJ, Tielens AGM, Friedrich T, Veenhuis M, Huynen MA, Hackstein JHP (2005) An anaerobic mitochondrion that produces hydrogen. Nature 434(7029):74–79
Distel DL (1998) Evolution of chemoautotrophic endosymbioses in bivalves. Bivalve-bacteria chemosymbioses are phylogenetically diverse but morphologically similar. BioScience 48:277–286
Doolittle WF (1998) You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet 14:307–311
Embley TM, Finlay BJ (1994) The use of small-subunit ribosomal-RNA sequences to unravel the relationships between anaerobic ciliates and their methanogen endosymbionts. Microbiology 140:225–235
Embley TM, Finlay BJ, Dyal PL, Hirt RP, Wilkinson M, Williams AG (1995) Multiple origins of anaerobic ciliates with hydrogenosomes within the radiation of aerobic ciliates. Proc R Soc Lond Ser B-Biol Sci 262(1363):87–93
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Fenchel T, Finlay BJ (1995) Ecology and evolution in anoxic worlds. Oxford University Press, New York
Fenchel T, Finlay BJ (2018) Free-living protozoa with endosymbiotic methanogens. In: Hackstein JHP (ed) (Endo)symbiotic methanogenic archaea. Springer, Heidelberg
Goosen NK, Horemans AMC, Hillebrand SJW, Stumm CK, Vogels GD (1988) Cultivation of the sapropelic ciliate Plagiopyla nasuta stein and isolation of the endosymbiont Methanobacterium formicicum. Arch Microbiol 150(2):165–170
Hackstein JHP, Tielens AGM (2018) Hydrogenosomes. In: Hackstein JHP (ed) (Endo)symbiotic methanogenic archaea. Springer, Heidelberg
Hackstein JHP, van Hoek AHAM, Leunissen JAM, Huynen M (2002) Anaerobic ciliates and their methanogenic endosymbionts. In: Seckbach J (ed) Symbiosis: mechanisms and model systems. Kluwer Academic Publishers, Dordrecht, pp 451–464. ISBN 1-4020-0189-4
Hirakata Y, Oshiki M, Kuroda K, Hatamoto M, Kubota K, Yamaguchi T, Harada H, Araki N (2015) Identification and detection of prokaryotic symbionts in the ciliate Metopus from anaerobic granular sludge. Microb Environ 30:335–338
Holmes DE, Giloteaux L, Orellana R, Williams KH, Robbins MJ, Lovley DR (2014) Methane production from protozoan endosymbionts following stimulation of microbial metabolism within subsurface sediments. Front Microbiol. https://doi.org/10.3389/fmicb.2014.00366
Krueger DM, Cavanaugh CM (1997) Phylogenetic diversity of bacterial symbionts of Solemya hosts based on comparative sequence analysis of 16S rRNA genes. Appl Environ Microbiol 63:91–98
Narayanan N, Krishnakumar B, Anupama VN, Manilal VB (2009) Methanosaeta sp., the major archaeal endosymbiont of Metopus es. Res Microbiol 160:600–607
Page RDM (1995) Paralell phylogenies: reconstructing the history of host-parasite assemblage. Cladistics 10:155–173
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Shinzato N, Watanabe I, Meng XY, Sekiguchi Y, Tamaki H, Matsui T, Kamagata Y (2007) Phylogenetic analysis and fluorescence in situ hybridization detection of archaeal and bacterial endosymbionts in the anaerobic ciliate Trimyema compressum. Microb Ecol 54:627–636
Shinzato N, Takeshita K, Kamagata Y (2018) The methanogenic and eubacterial endosymbionts of Trimyema. In: Hackstein JHP (ed) (Endo)symbiotic methanogenic archaea. Springer, Heidelberg
Ushida K (2018) Symbiotic methanogens and rumen ciliates. In: Hackstein JHP (ed) (Endo)symbiotic methanogenic archaea. Springer, Heidelberg
van Bruggen JJA, Zwart KB, van Assema RM, Stumm CK, Vogels GD (1984) Methanobacterium formicicum, an endosymbiont of the anaerobic ciliate Metopus striatus McMurrich. Arch Microbiol 139(1):1–7
van Bruggen JJA, Zwart KB, Hermans JGF, van Hove EM, Stumm CK, Vogels GD (1986) Isolation and characterization of Methanoplanus endosymbiosus sp.nov, an endosymbiont of the marine sapropelic ciliate Metopus contortus Quennerstedt. Arch Microbiol 144(4):367–374
van Hoek AHAM, Sprakel VSI, Van Alen TA, Theuvenet APR, Vogels GD, Hackstein JHP (1999) Voltage-dependent reversal of anodic galvanotaxis in Nyctotherus ovalis. J Eukaryot Microbiol 46(4):427–433
van Hoek AHAM, van Alen TA, Sprakel VSI, Leunissen JAM, Brigge T, Vogels GD, Hackstein JHP (2000) Multiple acquisition of methanogenic archaeal symbionts by anaerobic ciliates. Mol Biol Evol 17(2):251–258
Wagener S, Bardele CF, Pfennig N (1990) Functional integration of Methanobacterium formicicum into the anaerobic ciliate Trimyema compressum. Arch Microbiol 153:496–501
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Hackstein, J.H.P., de Graaf, R.M. (2018). Anaerobic Ciliates and Their Methanogenic Endosymbionts. In: Hackstein, J. (eds) (Endo)symbiotic Methanogenic Archaea. Microbiology Monographs, vol 19. Springer, Cham. https://doi.org/10.1007/978-3-319-98836-8_2
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