Fermentation products of the anaerobic ciliate Trimyema compressum in monoxenic cultures

Holler, Stephan; Pfennig, Norbert

doi:10.1007/bf00263006

Cited by 24 publications

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“…The introduced bacteria remained viable for at least two months but the symbiosis was again unstable, and the methanogens were lost within one week following stimulation of the host growth rate. Holler & Pfennig (1991) had a similar experience: their re-infected association was lost after two months. Interestingly, however, these authors dispelled any suggestion that the methanogens were only passive residents by showing that methane replaced formate as a major metabolic end-product when ' symbiotic' methanogens were introduced.…”

mentioning

confidence: 86%

A new polymorphic methanogen, closely related to Methanocorpusculum parvum, living in stable symbiosis within the anaerobic ciliate Trimyema sp.

Finlay

Embley

Fenchel

1993

Journal of General Microbiology

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(Received 13 July 1992; revised 23 September 1992; accepted 7 October 1992) A new anaerobic microbial consortium has been discovered: the partners are the ciliated protozoon Trimyema sp. and a single species of methanogen. The consortium has been maintained in culture for more than four years. Each ciliate contains up to 300 symbiotic bacteria; many are relatively small and irregularly disc-shaped, and these are distributed throughout the host's cytoplasm, whereas those which are attached to the ciliate's hydrogenosomes are significantly larger and profusely dentate. This attachment is interpreted as an adaptation to maximize capture by the bacteria of the H, escaping from hydrogenosomes. The 16s rRNA gene of the symbionts has been partially sequenced, and fluorescent oligonucleotide probes have been constructed and used to detect the different morphotypes of the symbiont within the ciliate. The symbionts belong to a new species of archaeobacterium which is a close relative of the free-living methanogen Methanocorpusculum paruum. IntroductionCiliates belonging to the genus Trimyema are all anaerobic : they were first recorded from sewage tanks (Lackey, 1925), and they are frequently encountered in anoxic freshwater habitats (e.g. Wagener et al., 1990 b). Some marine species are also known; T. echinometrae is an endocommensal of sea urchins (Grolikre et al., 1980). Trimyema compressum is frequently present in anoxic freshwater sediments. The ciliate was long known to harbour bacteria-sized particles in its cytoplasm (see Augustin et al., 1987) although the identity of these remained obscure until Wagener & Pfennig (1987) demonstrated that at least some of them were methanogenic bacteria. The same authors discovered that endosymbiotic methanogens were always present when the ciliates were freshly enriched from the natural environment. The methanogens were rod-shaped, variable in length (1.6-3-3 pm) and relatively wide (0.65 pm). The nucleotide sequence determined in this work has been submitted to EMBL and has been assigned the accession number 216412. symbionts occurred without apparent effect upon the growth of the host ciliates. Wagener et al. (1990a) then re-infected these aposymbiotic ciliates with two strains of methanogens isolated from other anaerobic ciliates. The introduced bacteria remained viable for at least two months but the symbiosis was again unstable, and the methanogens were lost within one week following stimulation of the host growth rate. Holler & Pfennig (1991) had a similar experience: their re-infected association was lost after two months. Interestingly, however, these authors dispelled any suggestion that the methanogens were only passive residents by showing that methane replaced formate as a major metabolic end-product when ' symbiotic' methanogens were introduced.Little else is known in detail concerning the anaerobic metabolism of Trimyema. It is clear, however, that in some strains at least, hydrogenase is present in the microbodies (Zwart et al., 1988; Goosen et al., 1990b;Bro...

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confidence: 86%

A new polymorphic methanogen, closely related to Methanocorpusculum parvum, living in stable symbiosis within the anaerobic ciliate Trimyema sp.

Finlay

Embley

Fenchel

1993

Journal of General Microbiology

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“…T. compressum strain N, for example, produced a large amount of lactate when Bacteroides sp. cells were fed, while it produced acetate when Rubrivivax gelatinosus cells were fed [9]. In another report, it was demonstrated that T. compressum produced ethanol predominantly under anaerobic conditions when Bacteroides sp.…”

Section: Discussionmentioning

confidence: 96%

“…It is known that endosymbiont‐free anaerobic ciliate cells often exist in natural habitats and monoxenic cultures [5, 9]. The significance of the endosymbionts for the growth efficiency of two ciliates, Plagiopyla frontata and Metopus contortus , was examined by inactivating methanogens with the specific methanogen inhibitor bromoethanesulfonic acid [10].…”

Section: Discussionmentioning

confidence: 99%

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The effect of endosymbiotic methanogens on the growth and metabolic profile of the anaerobic free-living ciliate Trimyema compressum

Yamada

Kamagata

Nakamura

2006

FEMS Microbiology Letters

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We examined the influence of endosymbiotic methanogens on the growth and metabolic profile of the anaerobic ciliate Trimyema compressum. When we isolated the ciliate, it possessed a large number of endosymbiotic Methanobacterium‐like methanogens inside the cell. The culture was transferred to fresh medium with Lactobacillus sp. cells as food bacteria. T. compressum grew to give a maximum cell number of 3300 cells/ml without loss of the endosymbionts over 30 passages of transfer. Acetate and methane were major end products with smaller amounts of propionate and butyrate. However, after further continued cultivation, the number of endosymbiotic methanogens started to decrease and they eventually disappeared. The growth and metabolic profile of the ciliate were changed significantly as the symbiotic association deteriorated. The major fermentation products were shifted to butyrate. These results suggest that the endosymbiotic methanogens which function as hydrogen scavengers are not indispensable for the growth and survival of T. compressum, although the growth yield decreased slightly in the absence of methanogens, and the ciliate is capable of fermenting food bacteria without endosymbiotic methanogens by changing its metabolic pathway.

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“…Measuring H 2 -production of aposymbiotic (previously BES-treated) cells could not, however, account for the CH 4 -production of cells with active methanogens: in Metopus the measured H 2 -production could account for about 70% of the CH 4 -production of normal cells and in Plagiopyla the corresponding figure was only about 45%. It is possible that some of the reduction equivalents produced by the hydrogenosomes is in the form of formate as has been shown for the anaerobic ciliate Trimyema (Goosen et al 1990;Holler and Pfennig 1991). This was not tested in Fenchel and Finlay (1991b), but it is likely that in the absence of methanogens, H 2 -tension will build up in the ciliates and thus inhibit H 2 -production in the hydrogenosomes which will instead excrete more reduced end products than acetate, such as lactate or propionate, and that the significance of the association between the host cells and their methanogenic symbionts is one of syntrophic H 2 -transfer (Worm et al 2010).…”

Section: Intracellular H 2 -Tension and Methanogensmentioning

confidence: 93%

Free-Living Protozoa with Endosymbiotic Methanogens

Fenchel

Finlay

2010

(Endo)symbiotic Methanogenic Archaea

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Fermentation products of the anaerobic ciliate Trimyema compressum in monoxenic cultures

Cited by 24 publications

References 22 publications

A new polymorphic methanogen, closely related to Methanocorpusculum parvum, living in stable symbiosis within the anaerobic ciliate Trimyema sp.

A new polymorphic methanogen, closely related to Methanocorpusculum parvum, living in stable symbiosis within the anaerobic ciliate Trimyema sp.

The effect of endosymbiotic methanogens on the growth and metabolic profile of the anaerobic free-living ciliate Trimyema compressum

Free-Living Protozoa with Endosymbiotic Methanogens

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