IJSEM Journal of Clinical Microbiology
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Supplementary Figure
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via CrossRef
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Hatamoto, M.
Right arrow Articles by Harada, H.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Hatamoto, M.
Right arrow Articles by Harada, H.
Agricola
Right arrow Articles by Hatamoto, M.
Right arrow Articles by Harada, H.
Int J Syst Evol Microbiol 57 (2007), 2137-2142; DOI  10.1099/ijs.0.64981-0
© 2007 International Union of Microbiological Societies

Syntrophomonas palmitatica sp. nov., an anaerobic, syntrophic, long-chain fatty-acid-oxidizing bacterium isolated from methanogenic sludge

Masashi Hatamoto1, Hiroyuki Imachi1,2, Sanae Fukayo1, Akiyoshi Ohashi1 and Hideki Harada1,3

1 Department of Environmental Systems Engineering, Nagaoka University of Technology, Nagaoka, Niigata 940-2188, Japan
2 Subground Animalcule Retrieval (SUGAR) Program, Extremobiosphere Research Center, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Kanagawa 237-0061, Japan
3 Department of Civil Engineering, Tohoku University, Sendai, Miyagi 980-8579, Japan

Correspondence
Hiroyuki Imachi
imachi{at}jamstec.go.jp


   ABSTRACT
TOP
 ABSTRACT
MAIN TEXT
 REFERENCES
 
A mesophilic, syntrophic, fatty-acid-oxidizing anaerobic strain, designated MPAT, was isolated from granular sludge in a mesophilic upflow anaerobic sludge blanket reactor used to treat palm oil mill effluent. Cells were slightly curved, non-motile rods. Spore formation was not observed. The optimal temperature for growth was around 37 °C and optimal pH for growth was 7.0. Strain MPAT was able to grow on crotonate or pentenoate plus butyrate in pure culture. In co-culture with the hydrogenotrophic methanogen Methanospirillum hungatei, strain MPAT was able to oxidize straight-chain saturated fatty acids with carbon chain lengths of C4–C18. The strain was unable to utilize sulfate, sulfite, thiosulfate, nitrate, fumarate, iron(III) or DMSO as an electron acceptor. The G+C content of the DNA was 45.0 mol%. Based on comparative 16S rRNA gene sequence analysis, strain MPAT was found to be a member of the genus Syntrophomonas and was most closely related to the type strains of Syntrophomonas curvata and Syntrophomonas sapovorans (sequence similarities of 94 %). Genetic and phenotypic characteristics demonstrated that strain MPAT represents a novel species, for which the name Syntrophomonas palmitatica sp. nov. is proposed. The type strain is MPAT (=JCM 14374T=NBRC 102128T=DSM 18709T).

Abbreviations: FAME, fatty acid methyl ester; LCFA, long-chain fatty acid

The GenBank/EMBL/DDBJ accession numbers for the rrnA and rrnB operons of the 16S rRNA gene sequence of strain MPAT are AB274039 and AB274040, respectively.

A phase-contrast micrograph showing the cell morphology of strain MPAT is available as supplementary material with the online version of this paper.


   MAIN TEXT
TOP
 ABSTRACT
 MAIN TEXT
REFERENCES
 
Natural lipids such as fats and oils are hydrolysed to long-chain fatty acids (LCFAs) and glycerol. Under methanogenic conditions, LCFAs are further degraded by the syntrophic association of LCFA-oxidizing, hydrogen (and/or formate)-producing fermentative bacteria and hydrogenotrophic methanogens, because the oxidation of LCFAs is thermodynamically unfavourable in such environments unless the consumption of hydrogen and/or formate is coupled with oxidation (Schink, 1997Go). Therefore, LCFA-degrading anaerobes can gain only a small amount of energy through these syntrophic reactions and thus their growth is generally slow. In addition, LCFAs can cause substrate toxicity in microbes. Consequently, isolation of LCFA-degrading bacteria has been difficult and, at the time of writing, only six species/subspecies have been described. Five of these belong to the family Syntrophomonadaceae within the phylum Firmicutes: Syntrophomonas sapovorans (Roy et al., 1986Go), Syntrophomonas wolfei subsp. saponavida (Lorowitz et al., 1989Go), Thermosyntropha lipolytica (Svetlitshnyi et al., 1996Go), Syntrophomonas curvata (Zhang et al., 2004Go) and the very recently described Syntrophomonas zehnderi (Sousa et al., 2007Go). There is only one species described to date belonging to the class Deltaproteobacteria, i.e. Syntrophus aciditrophicus (Jackson et al., 1999Go), which also degrades LCFAs syntrophically.

Recently, we successfully isolated strain MPAT from methanogenic granular sludge that was taken from palm oil mill effluent treated in a mesophilic upflow anaerobic sludge blanket reactor (Hatamoto et al., 2007Go). In a previous study, strain MPAT was found to be able to grow on palmitate in co-culture with the hydrogenotrophic methanogen Methanospirillum hungatei JF-1T (DSM 864T). Partial 16S rRNA gene sequence analysis revealed that strain MPAT was affiliated with the genus Syntrophomonas, but was only distantly related to any recognized species. In the present report, we describe the detailed morphological and physiological characteristics of strain MPAT and propose a novel species to accommodate it.

Strain MPAT was isolated from a methanogenic granular sludge by using conventional techniques combined with in situ hybridization detection via a 16S rRNA-targeted fluorescently labelled oligonucleotide probe (Hatamoto et al., 2007Go). Media for cultivation of strain MPAT were prepared as described by Sekiguchi et al. (2000Go). Strain MPAT formed small, white–brownish lens-shaped colonies of 0.5–1 mm in diameter on agar roll tube medium with 20 mM crotonate after 1 month incubation. Cell morphologies were observed under a fluorescent microscope (Olympus BX50F). Cells of strain MPAT were non-motile, curved rods 1.5–4.0 µm long and 0.4–0.6 µm wide with round ends (see Supplementary Fig. S1 in IJSEM Online). Cells were Gram-negative according to the method of Hucker (Doetsch, 1981Go). Spores were not observed in pure culture or co-culture with M. hungatei.

Strain MPAT was strictly anaerobic as no growth occurred under trace quantities of oxygen [0.1 and 0.2 % O2 (v/v)]. Growth in pure culture was observed on crotonate or butyrate plus pentenoate as an energy source. Yeast extract (0.05 %) was not required but did stimulate growth. For determination of the fermentation products of strain MPAT, we used a GC-TCD (gas chromatograph equipped with thermal conductivity detector) and GC-FID (gas chromatograph equipped with flame ionization detector) as described by Kucivilize et al. (2003Go), and HPLC as described by Imachi et al. (2002Go). Fermentation products from crotonate were butyrate and acetate; 1 mol crotonate was converted to 0.2 mol butyrate and 1.5 mol acetate after 14 days (90 % electron recovery). During incubation with crotonate in pure culture, hydrogen was always below 30 Pa in the gas phase. The following substrates did not serve as sole carbon and energy source (increase of turbidity was not observed after 3 months incubation, duplicate cultures): yeast extract (0.2 %), tryptone (0.2 %), Casamino acids (0.2 %), glucose (10 mM), sucrose (10 mM), ribose (10 mM), xylose (10 mM), acetate (20 mM), propionate (10 mM), butyrate (20 mM), iso-butyrate (20 mM), straight-chain fatty acids from C5 to C8 (5 mM), straight-chain fatty acids from C10 to C18 (1 mM+1 mM CaCl2), oleate (1 mM) plus CaCl2 (1 mM), linoleate (1 mM) plus CaCl2 (1 mM), pentenoate (10 mM), fumarate (10 mM), malate (10 mM), succinate (10 mM), formate (10 mM), lactate (10 mM), glycerol (5 mM), ethanol (10 mM), 1-propanol (10 mM) and benzoate (5 mM). The following were tested as electron acceptors with butyrate (20 mM) and yeast extract (0.05 %) as electron donor, but none of them was utilized: sulfate (20 mM), sulfite (2 mM), thiosulfate (20 mM), nitrate (20 mM), fumarate (20 mM), iron(III)-nitrilotriacetate (5 mM) and DMSO (10 mM).

Substrate utilization of strain MPAT in co-culture with M. hungatei was investigated for the same substrates used in the pure culture study. Only the following substrates were used and produced methane within 3 months of cultivation: butyrate (20 mM), straight-chain saturated fatty acids from C5 to C8 (5 mM), straight-chain saturated fatty acids from C10 to C18 (1 mM+1 mM CaCl2) and pentenoate (10 mM). As shown in Fig. 1Go, palmitate was completely degraded and transformed into acetate and methane within 2 weeks of incubation in co-culture with M. hungatei (106 % electron recovery). The growth rate of the strain in co-culture with M. hungatei on palmitate (1 mM) was approximately 1.2 day–1 (determined by measuring methane production). Fatty acids with an even number of carbon atoms were converted into acetate and methane, whereas those with an odd number of carbon atoms were converted into propionate and methane, implying that beta-oxidation of fatty acids was performed by the co-culture.


Figure 1
View larger version (23K):
[in this window]
[in a new window]

  		Fig. 1. Degradation of palmitate and production of acetate, methane and hydrogen by strain MPAT in co-culture with M. hungatei JF-1T.

 
Effects of pH, temperature and NaCl on growth rate were determined by using the basal medium containing 10 mM crotonate plus 0.05 % yeast extract with 2 % (v/v) inoculum. Growth rate was determined by measuring the OD600. To determine the optimum pH for strain MPAT, the initial pH of the crotonate medium was adjusted to 5.5–9.0 by adding HCl or NaOH under a 100 % N2 atmosphere at room temperature, and the strain was then incubated at 37 °C in triplicate. Under these conditions, the pH range for growth was 6.5–8.0 with optimum growth at pH 7.0. For determinations of the optimum temperature for growth, cultures were incubated at 25, 30, 35, 37, 40, 45, 50 and 55 °C in duplicate. The strain grew optimally at 37 °C; no growth was observed at 25 or 55 °C. The NaCl tolerance concentration range was 1–200 mM (growth was improved at below 25 mM NaCl) determined in duplicate incubations. Under optimum conditions (pH 7.0, 37 °C), the growth rate of the strain in pure culture on crotonate was 1.07±0.02 day–1 (triplicate determinations). This growth rate was about the same order as that of Syntrophomonas wolfei subsp. wolfei or the thermophilic species Syntrophothermus lipocalidus [0.7 and 0.9 day–1, respectively (Beaty & McInerney, 1987Go; Sekiguchi et al., 2000Go)] but was slower than that for Syntrophomonas curvata (2.2 day–1; Zhang et al., 2004Go).

The effect of antibiotics on growth of strain MPAT was tested under optimum cultivation conditions by using 10 mM crotonate supplemented with 0.05 % yeast extract as a substrate. The strain was able to tolerate ampicillin (50 µg ml–1), but rifampicin, chloramphenicol, kanamycin, neomycin and vancomycin (all at 50 µg ml–1) completely inhibited growth.

For determination of the DNA base composition, DNA was extracted and purified according to the method of Kamagata & Mikami (1991Go). The DNA G+C content of strain MPAT was 45.0 mol%, as determined by direct analysis of deoxyribonucleotides by HPLC (Tamaoka & Komagata, 1984Go). For fatty acid methyl ester (FAME) analysis, cells of strain MPAT grown on 20 mM crotonate plus 0.05 % yeast extract were harvested. Extraction of cellular fatty acids and methylation were performed as described by Takai et al. (2004)Go. The FAMEs were analysed via GC-MS (TRACE GC ULTRA+DSQ system; Thermo electron). The major fatty acids of strain MPAT were C14 : 0 (27.1 % of total fatty acids), C16 : 0 (19.8 %), C18 : 0 (17.5 %), C16 : 1 (15.9 %), C15 : 0 (7.7 %) and C18 : 1 (3.8 %).

Directly extracted DNA from a pure culture of strain MPAT was used for amplification of the 16S rRNA gene by using bacterial 8f and universal 1490r primer sets (Weisburg et al., 1991Go) and sequenced by using the methods of Qiu et al. (2004Go). Sequencing results revealed that in the V1 region of the 16S rRNA gene sequence fragment peaks overlapped, suggesting that several sequences existed, but the rest of the 16S rRNA gene sequences were unambiguous. We therefore speculated that strain MPAT has sequence heterogeneities in the rrn operons. The PCR products were purified with a MinElute PCR purification kit (Qiagen), followed by cloning with a TOPO TA cloning kit (Invitrogen). Ten clonal rRNA genes were randomly picked and sequenced. We found two types of 16S rRNA gene sequences and these were identical except for the V1 region. We designated the shorter sequence as rrnA (1571 bp, 6/10 clones) and the longer one as rrnB (1589 bp, 4/10 clones). Although we repeatedly isolated strain MPAT by single colony isolation from roll tubes, there is a slight possibility that two closely related species were isolated. To exclude this possibility, fluorescence in situ hybridization was applied for both sequences in individual cells. Two fluorescently labelled oligonucleotide probes specific to each rrn sequence were designed to determine whether the rrnA and rrnB sequences belonged to a single cell. However, for a variety of hybridization conditions, we were unable to detect positive signals from these newly designed probes (data not shown), despite observing hybridization of a previously designed strain MPAT-targeted probe MPA1446 (Hatamoto et al., 2007Go). This could be due to the relative accessibility of the target sites (Amann et al., 1995Go). Alternatively, the 16S rRNA gene target may not be transcribed, as in Clostridium paradoxum (Rainey et al., 1996Go), or the target may be transcribed but excised during rRNA maturation (Evguenieva-Hackenberg, 2005Go). Consequently, we confirmed the 16S rRNA gene sequence of strain MPAT. We extracted total RNA, by using the method described by Sekiguchi et al. (2005Go), from crotonate-grown cultures of strain MPAT and this was reverse transcribed by using SuperScript III Reverse Transcriptase (Invitrogen) with a primer complementary to the 530f primer (Lane, 1991Go). The resulting cDNA was used for PCR amplification with the 8f/530r primer set and the products were sequenced. Only the 16S rRNA gene sequence of rrnA was detected, suggesting that strain MPAT has one type of 16S rRNA. Based on these results, and given the fact that multiple numbers and heterogeneity of 16S rRNA genes are common phenomena (Acinas et al., 2004Go), we conclude that strain MPAT has two types of 16S rRNA gene sequence but that only the rrnA type of 16S rRNA was transcribed.

Comparative 16S rRNA gene sequence phylogenetic analysis was performed as described by Hatamoto et al. (2007Go). Bootstrap resampling analysis was performed with the neighbour-joining, maximum-parsimony and maximum-likelihood methods to estimate the confidence of tree topologies, as described by Sekiguchi et al. (2006Go). A phylogenetic tree including rrnA and rrnB 16S rRNA gene sequences of strain MPAT and other members of the family Syntrophomonadaceae was constructed (Fig. 2Go). The phylogenetic analysis indicated that strain MPAT was affiliated with the genus Syntrophomonas. The closest relatives of strain MPAT were the type strains of Syntrophomonas curvata and Syntrophomonas sapovorans (both having similarity values of 94 % for rrnA and rrnB).


Figure 2
View larger version (38K):
[in this window]
[in a new window]

  		Fig. 2. Phylogenetic position of strain MPAT and related organisms. The tree was calculated based on a distance matrix analysis of 16S rRNA gene sequences (neighbour-joining tree). The 16S rRNA gene sequence of Arthrobacter globiformis DSM 20124T (X80736) was used to root the tree (not shown). Branching points supported with probabilities above 90 % by all the analyses (based on 1000 replicates, estimated by using the neighbour-joining, maximum-parsimony and maximum-likelihood methods) are indicated by a solid circle, whereas nodes with open circles indicate >70 % bootstrap probability support by the three analyses. The accession number of each reference sequence is shown in parentheses. Bar, 0.05 nucleotide changes per sequence position.

 
Based on these results, strain MPAT is considered to represent a member of the genus Syntrophomonas. Strain MPAT and other Syntrophomonas species share common phenotypic features (Table 1Go), particularly syntrophic growth with hydrogenotrophic methanogens on short-chain fatty acids and the inability to utilize external electron acceptors. However, strain MPAT differs from Syntrophomonas curvata and Syntrophomonas sapovorans in growth temperature and pH range for growth (Table 1Go). The FAME profile of strain MPAT differed from those of other Syntrophomonas species, with strain MPAT having C18 : 0 as one of the predominant fatty acids (Henson et al., 1988Go; Zhang et al., 2004Go, 2005Go). Although strain MPAT has almost the same substrate range as Syntrophomonas curvata, the mechanism of degradation of crotonate in pure culture is different, i.e. Syntrophomonas curvata converts 1 mol crotonate to 0.5 mol butyrate and 1 mol acetate (Zhang et al., 2004Go). By contrast, strain MPAT converts 1 mol crotonate to 0.2 mol butyrate and 1.5 mol acetate, similar to Syntrophomonas wolfei subsp. wolfei. However, Syntrophomonas wolfei subsp. wolfei is unable to degrade LCFAs in co-culture with methanogens, whereas strain MPAT can (Table 1Go). Based on the phenotypic features of strain MPAT as well as its 16S rRNA gene sequence divergence, we consider that strain MPAT represents a novel species of the genus Syntrophomonas, for which the name Syntrophomonas palmitatica sp. nov. is proposed.


View this table:
[in this window]
[in a new window]

  		Table 1. Characteristics of strain MPAT (Syntrophomonas palmitatica sp. nov.) and related organisms in the family Syntrophomonadaceae

Reference strains: 1, Syntrophomonas sapovorans OMT (data from Roy et al., 1986Go; Zhang et al., 2005Go); 2, Syntrophomonas curvata GB8-1T (Zhang et al., 2004Go, 2005Go); 3, Syntrophomonas saponavida SD2T (Lorowitz et al., 1989Go); 4, Syntrophomonas wolfei subsp. wolfei DSM 2245T (McInerney et al., 1979Go, 1981Go; Beaty & McInerney, 1987Go; Zhang et al., 2005Go); 5, Syntrophomonas bryantii CuCa1T (Stieb & Schink, 1985Go; Zhao et al., 1990Go; Wu et al., 2006Go). In co-culture with methanogens, all strains can use straight-chain fatty acids with butyrate to caprylate, whereas all strains cannot use propionate. ND, Not determined; –, negative; +, positive; ±, variable.

 
Description of Syntrophomonas palmitatica sp. nov.
Syntrophomonas palmitatica (pal.mi.ta'ti.ca. N.L. n. palmitas -atis palmitate; L. suff. -icus -a -um suffix used with the sense of belonging to; N.L. fem. adj. palmitatica belonging to palmitate).

Cells are slightly curved rods, 1.5–4.0 µm long and 0.4–0.6 µm wide. Strictly anaerobic and Gram-negative. Can grow in pure culture on crotonate or pentenoate plus butyrate. Does not utilize sulfate, sulfite, thiosulfate, nitrate, fumarate, iron(III)-nitrilotriacetate or DMSO as electron acceptors. In syntrophic association with hydrogenotrophic methanogens, can utilize straight-chain saturated fatty acids with 4–18 carbon atoms. Acetate, propionate, iso-butyrate and benzoate do not support growth of the co-culture. Temperature range for growth is 30–50 °C (optimum, 37 °C). pH range for growth is 6.5–8.0 (optimum, pH 7.0). The G+C content of the DNA of the type strain is 45.0 mol%.

The type strain, MPAT (=JCM 14374T=NBRC 102128T=DSM 18709T), was isolated from granular sludge of an upflow anaerobic sludge blanket reactor treating palm oil mill effluent.


   ACKNOWLEDGEMENTS
 
We thank Satoshi Nakagawa and Masayuki Miyazaki at JAMSTEC for FAME analysis and measurement of DNA G+C contents, respectively. We also thank Diana Z. Sousa at the University of Minho for providing sequence information of Syntrophomonas zhenderi. This study was financially supported by the New Energy and Industrial Technology Development Organization (NEDO), Japan Society for the Promotion of Science, Institute for Fermentation, Osaka, and the 21st Century COE program ‘Global Renaissance by Green Energy Revolution’ subsidized by the Japanese Ministry of Education, Culture, Sports, Science and Technology, Tokyo, Japan.


   REFERENCES
TOP
 ABSTRACT
 MAIN TEXT
 REFERENCES
 
Acinas, S. G., Marcelino, L. A., Klepac-Ceraj, V. & Polz, M. F. (2004). Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. J Bacteriol 186, 2629–2635.[Abstract/Free Full Text]

Amann, R. I., Ludwig, W. & Schleifer, K. H. (1995). Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59, 143–169.[Abstract/Free Full Text]

Beaty, P. S. & McInerney, M. J. (1987). Growth of Syntrophomonas wolfei in pure culture on crotonate. Arch Microbiol 147, 389–393.[CrossRef]

Doetsch, R. N. (1981). Determinative methods of light microscopy. In Manual of Methods for General Bacteriology, pp. 21–33. Edited by P. Gerhardt, R. G. E. Murray, R. N. Costilow, E. W. Nester, W. A. Wood, N. R. Krieg & G. B. Phillips. Washington, DC: American Society for Microbiology.

Evguenieva-Hackenberg, E. (2005). Bacterial ribosomal RNA in pieces. Mol Microbiol 57, 318–325.[CrossRef][Medline]

Hatamoto, M., Imachi, H., Ohashi, A. & Harada, H. (2007). Identification and cultivation of anaerobic, syntrophic long-chain fatty acid degrading microbes from mesophilic and thermophilic methanogenic sludges. Appl Environ Microbiol 73, 1332–1340.[Abstract/Free Full Text]

Henson, J. M., McInerney, M. J., Beaty, P. S., Nickels, J. & White, D. C. (1988). Phospholipid fatty acid composition of the syntrophic anaerobic bacterium Syntrophomonas wolfei. Appl Environ Microbiol 54, 1570–1574.[Abstract/Free Full Text]

Imachi, H., Sekiguchi, Y., Kamagata, Y., Hanada, S., Ohashi, A. & Harada, H. (2002). Pelotomaculum thermopropionicum gen. nov., sp. nov., an anaerobic, thermophilic, syntrophic propionate-oxidizing bacterium. Int J Syst Evol Microbiol 52, 1729–1735.[Abstract]

Jackson, B. E., Bhupathiraju, V. K., Tanner, R. S., Woese, C. R. & McInerney, M. J. (1999). Syntrophus aciditrophicus sp. nov., a new anaerobic bacterium that degrades fatty acids and benzoate in syntrophic association with hydrogen-using microorganisms. Arch Microbiol 171, 107–114.[CrossRef][Medline]

Kamagata, Y. & Mikami, E. (1991). Isolation and characterization of a novel thermophilic Methanosaeta strain. Int J Syst Bacteriol 41, 191–196.[Abstract/Free Full Text]

Kucivilize, P., Ohashi, A. & Harada, H. (2003). Process performance and sludge behaviors of multi-staged UASB reactor for treatment of palm oil mill effluent (POME). Environ Eng Res 40, 441–449 (in Japanese)

Lane, D. J. (1991). 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematics, pp. 115–175. Edited by E. Stackebrandt & M. Goodfellow. Chichester: Wiley.

Lorowitz, W. H., Zhao, H. & Bryant, M. P. (1989). Syntrophomonas wolfei subsp. saponavida subsp. nov., a long-chain fatty-acid-degrading, anaerobic, syntrophic bacterium; Syntrophomonas wolfei subsp. wolfei subsp. nov.; and emended descriptions of the genus and species. Int J Syst Bacteriol 39, 122–126.[Abstract/Free Full Text]

McInerney, M. J., Bryant, M. P. & Pfennig, N. (1979). Anaerobic bacterium that degrades fatty acids in syntrophic association with methanogens. Arch Microbiol 122, 129–135.[CrossRef]

McInerney, M. J., Bryant, M. P., Hespell, R. B. & Costerton, J. W. (1981). Syntrophomonas wolfei gen. nov. sp. nov., an anaerobic, syntrophic, fatty acid-oxidizing bacterium. Appl Environ Microbiol 41, 1029–1039.[Abstract/Free Full Text]

Qiu, Y. L., Sekiguchi, Y., Imachi, H., Kamagata, Y., Tseng, I. C., Cheng, S. S., Ohashi, A. & Harada, H. (2004). Identification and isolation of anaerobic, syntrophic phthalate isomer-degrading microbes from methanogenic sludges treating wastewater from terephthalate manufacturing. Appl Environ Microbiol 70, 1617–1626.[Abstract/Free Full Text]

Rainey, F. A., Ward-Rainey, N. L., Janssen, P. H., Hippe, H. & Stackebrandt, E. (1996). Clostridium paradoxum DSM 7308T contains multiple 16S rRNA genes with heterogeneous intervening sequences. Microbiology 142, 2087–2095.[Abstract/Free Full Text]

Roy, F., Samain, E., Dubourguier, H. C. & Albagac, G. (1986). Syntrophomonas sapovorans sp. nov., a new obligately proton reducing anaerobe oxidizing saturated and unsaturated long chain fatty acids. Arch Microbiol 145, 142–147.[CrossRef]

Schink, B. (1997). Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev 61, 262–280.[Abstract]

Sekiguchi, Y., Kamagata, Y., Nakamura, K., Ohashi, A. & Harada, H. (2000). Syntrophothermus lipocalidus gen. nov., sp. nov., a novel thermophilic, syntrophic, fatty-acid-oxidizing anaerobe which utilizes isobutyrate. Int J Syst Evol Microbiol 50, 771–779.[Abstract]

Sekiguchi, Y., Uyeno, Y., Sunaga, A., Yoshida, H. & Kamagata, Y. (2005). Sequence-specific cleavage of 16S rRNA for rapid and quantitative detection of particular groups of anaerobes in bioreactors. Water Sci Technol 52, 107–113.[Medline]

Sekiguchi, Y., Imachi, H., Susilorukmi, A., Muramatsu, M., Ohashi, A., Harada, H., Hanada, S. & Kamagata, Y. (2006). Tepidanaerobacter syntrophicus gen. nov., sp. nov., an anaerobic, moderately thermophilic, syntrophic alcohol- and lactate-degrading bacterium isolated from thermophilic digested sludges. Int J Syst Evol Microbiol 56, 1621–1629.[Abstract/Free Full Text]

Sousa, D. Z., Smidt, H., Alves, M. M. & Stams, A. J. M. (2007). Syntrophomonas zehnderi sp. nov., an anaerobe that degrades long chain fatty acids in co-culture with Methanobacterium formicicum. Int J Syst Evol Microbiol 57, 609–615.[Abstract/Free Full Text]

Stieb, M. & Schink, B. (1985). Anaerobic oxidation of fatty acids by Clostridium bryantii sp. nov., a sporeforming, obligately syntrophic bacterium. Arch Microbiol 140, 387–390.[CrossRef]

Svetlitshnyi, V., Rainey, F. & Wiegel, J. (1996). Thermosyntropha lipolytica gen. nov., sp. nov., a lipolytic, anaerobic, alkalitolerant, thermophilic bacterium utilizing short- and long-chain fatty acids in syntrophic coculture with a methanogenic archaeum. Int J Syst Bacteriol 46, 1131–1137.[Abstract/Free Full Text]

Takai, K., Nealson, K. H. & Horikoshi, K. (2004). Hydrogenimonas thermophila gen. nov., sp. nov., a novel thermophilic, hydrogen-oxidizing chemolithoautotroph within the {epsilon}-Proteobacteria, isolated from a black smoker in a Central Indian Ridge hydrothermal field. Int J Syst Evol Microbiol 54, 25–32.[Abstract/Free Full Text]

Tamaoka, J. & Komagata, K. (1984). Determination of DNA base composition by reversed-phase high-performance liquid chromatography. FEMS Microbiol Lett 25, 125–128.[CrossRef]

Weisburg, W. G., Barns, S. M., Pelletier, D. A. & Lane, D. J. (1991). 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173, 697–703.[Abstract/Free Full Text]

Wu, C., Liu, X. & Dong, X. (2006). Syntrophomonas cellicola sp. nov., a spore-forming syntrophic bacterium isolated from a distilled-spirit-fermenting cellar, and assignment of Syntrophospora bryantii to Syntrophomonas bryantii comb. nov. Int J Syst Evol Microbiol 56, 2331–2335.[Abstract/Free Full Text]

Zhang, C., Liu, X. & Dong, X. (2004). Syntrophomonas curvata sp. nov., an anaerobe that degrades fatty acids in co-culture with methanogens. Int J Syst Evol Microbiol 54, 969–973.[Abstract/Free Full Text]

Zhang, C., Liu, X. & Dong, X. (2005). Syntrophomonas erecta sp. nov., a novel anaerobe that syntrophically degrades short-chain fatty acids. Int J Syst Evol Microbiol 55, 799–803.[Abstract/Free Full Text]

Zhao, H. X., Yang, D. C., Woese, C. R. & Bryant, M. P. (1990). Assignment of Clostridium bryantii to Syntrophospora bryantii gen. nov., comb. nov. on the basis of a 16S rRNA sequence analysis of its crotonate-grown pure culture. Int J Syst Bacteriol 40, 40–44.[Abstract/Free Full Text]





This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Supplementary Figure
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via CrossRef
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Hatamoto, M.
Right arrow Articles by Harada, H.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Hatamoto, M.
Right arrow Articles by Harada, H.
Agricola
Right arrow Articles by Hatamoto, M.
Right arrow Articles by Harada, H.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
INT J SYST EVOL MICROBIOL MICROBIOLOGY J GEN VIROL
J MED MICROBIOL ALL SGM JOURNALS