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Methanothrix Spp. ALBERTO J JOURNAL OF BACTERIOLOGY, Sept. 1987, p. 4099-4103 Vol. 169, No. 9 0021-9193/87/094099-05$02.00/0 Copyright © 1987, American Society for Microbiology Antigenic Distinctiveness, Heterogeneity, and Relationships of Methanothrix spp. ALBERTO J. L. MACARIO* AND EVERLY CONWAY DE MACARIO Wadsworth Center for Laboratories and Research and School of Public Health Sciences, New York State Department of Health, and State University of New York, Albany, New York 12201 Received 23 March 1987/Accepted 1 June 1987 A detailed immunologic analysis of Methanothrir soehngenii Opfikon (the type species of the genus), Methanothrix sp. strain CALS-1, and Methanothrix concilii GP6 was performed. A variety of poly- and monoclonal antibody probes for a comprehensive panel of reference organisms were used to determine immunogenicity, antigenicity, and relationships. The three organisms are antigenically distinct but interre- lated, forming an immunologically cohesive group, weakly related to methanosarcinae. A prominent feature of the organisms was heterogeneity characterized by antigenic diversity and compartmentation, the latter particularly evident in M. soehngenii Opfikon, which was examined more thoroughly. The complexity of the antigenic profile of this strain and the heterogeneity of the group suggest a high degree of phenotypic diversification within the genus. Acetic acid is the precursor of at least two-thirds of the ganisms at the immunotype level. These means and funda- methane produced in most anaerobic ecosystems (9, 13, 18). mental data on the diversity of Methanothrix organisms are Acetate utilization likely constitutes the rate-limiting step in described in this report. the anaerobic conversion of organic matter to methane. In this bioconversion, aceticlastic methanogens play a key role. MATERIALS AND METHODS However, these microorganisms are not yet well character- Bacteria. M. soehngenii Opfikon was provided by H. P. ized. The few species of aceticlastic methanogens that have Kohler, Methanothrix sp. strain CALS-1 by S. H. Zinder, been identified have been assigned to two genera, Methano- and M. concilii GP6 by G. B. Patel. The reference sarcina and Methanothrix (1, 7, 9, 13, 15). methanogens in our panel of antigens (4, 5, 11, 12) were: 1, Methanothrix organisms appear as sheathed filaments Methanobrevibacter smithii PS; 2, Methanobacterium with spacer plugs between cells, superficially resembling formicicum MF; 3, Methanosarcina barkeri MS; 4, Methanospirillum filaments although the ultrastructure of Methanobacterium bryantii MoH; 5, Methanobacterium the spacer plugs is different in the two genera (14). Only bryantii MoHG; 6, Methanosarcina barkeri R1M3; 7, three organisms of the genus Methanothrix have been de- Methanospirillum hungatei (Methanospirillum hungatii) scribed in detail, Methanothrix soehngenii, the type species JF1; 8, Methanobrevibacter ruminantium Ml; 9, Methano- (9, 16), M. concilii (3, 13), and Methanothrix sp. strain brevibacter arboriphilus (Methanobrevibacter arbori- CALS-1 (17). One reason for the scarcity of knowledge philicus) DH1; 10, Methanobrevibacter smithii ALI; 11, about Methanothrix organisms is that they are difficult to Methanobacterium thermoautotrophicum GC1; 12, Meth- cultivate. They have long generation times and low cell anobacterium thermoautotrophicum AH; 13, Meth- yields (2, 3, 9, 13, 16). anococcus vannielii SB; 14, Methanococcus voltae PSv; 15, A comprehensive survey of ecosystems of interest to Methanogenium marisnigri JR1; 16, Methanosarcina determine Methanothrix species would be impracticable barkeri 227; 17, Methanogenium cariaci JR1; 18, Meth- with current techniques. Morphotypes resembling Methano- anosarcina mazei S6; 19, Methanosarcina barkeri W; 20, thrix organisms are frequently seen in digestor contents and Methanosarcina thermophila TM1; 21, Methanobrevibacter enrichment cultures viewed microscopically (16, 17). These arboriphilus (Methanobrevibacter arboriphilicus) AZ; 22, morphotypes are difficult to identify since they do not Methanobrevibacter arboriphilus (Methanobrevibacter autofluoresce (16-18) as methanogens in general do (1). arboriphilicus) DC; 23, Methanomicrobium mobile BP; 24, Moreover, rapid elucidation of whether all Methanothrix- Methanothermusfervidus V24S; 25, Methanolobus tindarius like rods in a mixture are of the same or different species is T3; 26, Methanococcus maripaludis WJJ; 27, Methano- unfeasible. These organisms are difficult to isolate, as it is sphaera stadtmaniae MCB3; 28, Methanoplanus limicola not always clear whether a viable unit represents a single cell M3; and 29, Methanococcus thermolithotrophicus SN1. or an aggregate of many cells (16-18). Animals, immunizations, antisera, and polyclonal and These technical limitations must be overcome to advance monoclonal antibody probes. Rabbits and mice were immu- knowledge of these methanogenic bacteria which hold nized with M. soehngenii Opfikon or with Methanothrix sp. biotechnologic potential and are scientifically very interest- strain CALS-1. The bacterial preparations were judged well ing (1-3, 7, 9, 13-16, 18). Tools are needed to determine preserved and devoid of contamination by microscopy rapidly Methanothrix species and strains in any given eco- (phase-contrast and bright-field optics of unstained and system and to quantify each group. Gram-stained preparations, respectively) and immunologic We developed immunologic means to allow structural screening with the panel of antibody probes for reference determinations and rapid identification of Methanothrix or- methanogens. The immune sera were obtained and banked as described previously (10, 11). Special schedules and * Corresponding author. antigen preparations were used to investigate immunogenic- 4099 4100 MACARIO AND CONWAY DE MACARIO J. BACTERIOL. TABLE 1. Comparison of serum antibody responses of rabbits idase for SIA). The results always showed low antibody immunized with Methanothrix spp. titers in sera from animals immunized with strain Opfikon, Antigen Serum (bleeding) although somewhat brighter IIF reactions were obtained Rabbit Dose Days after Antibody when incubations were done at 37°C rather than at the Strain temperature routinely used, i.e., 25°C. No.no.la* ast dose titerb (iii) Topography of surface antigens. The pattern of IIF A M. soehngenii 2 1 14 3,200 reaction of CALS-1 was different from that of Opfikon. Opfikon 3 2 11 3,200 CALS-1 displayed a homogeneous, solid, bright reaction 3 18 3,200 pattern typical of methanogenic bacilli (Fig. la). The reac- B M. soehngenii 2 1 14 3,200 tion more intense on the and of Opfikon 3 2 16 3,200 appeared edges tips the rods 3 32 3,200 at high antiserum dilutions. Strain Opfikon, on the contrary, 4 4 13 6,400 showed a solid, homogeneous reaction pattern only occa- 5 20 6,400 sionally. A discontinuous reaction was the rule, with slight 5c 6 10 12,800 variations depending on the antiserum and dilution tested. A C Methanothrix 2 1 14 >102,000 succession of narrow bands perpendicular to the long axis of sp. strain 2 25 >102,000 the rods was observed (Fig. lb). Another common pattern CALS-1 3 3 14 >102,000 consisted of short positive segments separated by negative 4 22 >102,000 ones, forming a dashed line on each side of the rod from one 5 29 >102,000 end to the other (Fig. lc). This was occasionally accompa- 6 37 >102,000 nied by a dot or by a "plug" of fluorescence on each end of a Whole bacterial cells, formalinized and emulsified in Freund complete the rods. In addition to these positive spots, some antisera adjuvant, were given for the first two doses; similarly treated cells but without produced solid reaction segments of various lengths and adjuvant were given for the following doses, all subcutaneously (except where indicated). numbers, distributed at intervals on the rods. Some antisera bReciprocal of serum dilution giving the last positive reading of the titration produced still another pattern of IIF reaction. This consisted curve. of fine granules densely spread over the length of the rods, c Cell-free supernatant of strain Opfikon cell suspension given intra- which resembled narrow strips of frosted glass (Fig. ld). venously. Specificity spectra of antibody probes for strains Opfikon and CALS-1. Due to the peculiar IIF-reaction morphology of ity as specified in Results. Monoclonal antibodies were the strain Opfikon, the S probe for this strain was defined as prepared by standard procedures. the last antiserum dilution in the titration curve's plateau Assays. The quantitative slide immunoenzymatic assay evaluating the reaction on the positive spots, rather than on (SIA), the immunoenzymatic assay in suspension, adsorp- the whole cell. tion tests, and indirect immunofluorescence (IIF) were done The specificity spectra of the S probes for the two strains as described previously (5, 6, 11, 12). IIF photography was were determined by assaying them with the 29 reference performed when the intensity of the fluorescence allowed. methanogens listed in Materials and Methods. No reaction Determinations of specificity spectrum of polyclonal anti- was observed. body probes, antigenic fingerprints, and antigenic relation- Antigenic relationships of Methanothruc spp. The results of ships were done as described previously (10-12). testing the three Methanothrix organisms with the S probes for strains Opfikon and CALS-1 are shown in Table 2. No RESULTS cross-reactions were detected by quantitative SIA. These results were confirmed using six mouse antisera against Characterization of strains
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