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Non-Sulfate-Reducing, Syntrophic Bacteria Affiliated with Desulfotomaculum Cluster I Are Widely Distributed in Methanogenic Envi

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Non-Sulfate-Reducing, Syntrophic Bacteria Affiliated with Desulfotomaculum Cluster I Are Widely Distributed in Methanogenic Envi APPLIED AND ENVIRONMENTAL MICROBIOLOGY, Mar. 2006, p. 2080–2091 Vol. 72, No. 3 0099-2240/06/$08.00ϩ0 doi:10.1128/AEM.72.3.2080–2091.2006 Copyright © 2006, American Society for Microbiology. All Rights Reserved. Non-Sulfate-Reducing, Syntrophic Bacteria Affiliated with Desulfotomaculum Cluster I Are Widely Distributed in Methanogenic Environments Hiroyuki Imachi,1* Yuji Sekiguchi,1,2 Yoichi Kamagata,1,2 Alexander Loy,3 Yan-Ling Qiu,1,2 Downloaded from Philip Hugenholtz,4 Nobutada Kimura,2 Michael Wagner,3 Akiyoshi Ohashi,1 and Hideki Harada1 Department of Environmental Systems Engineering, Nagaoka University of Technology, Nagaoka, Niigata 940-2188, Japan1; Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science and Technology (AIST) Center 6, Tsukuba, Ibaraki 305-8566, Japan2; Department of Microbial Ecology, University of Vienna, A-1090 Vienna, Austria3; and Microbial Ecology Program, DOE Joint Genome Institute, Walnut Creek, California4 Received 16 November 2005/Accepted 27 December 2005 http://aem.asm.org/ The classical perception of members of the gram-positive Desulfotomaculum cluster I as sulfate-reducing bacteria was recently challenged by the isolation of new representatives lacking the ability for anaerobic sulfate respiration. For example, the two described syntrophic propionate-oxidizing species of the genus Pelotomacu- lum form the novel Desulfotomaculum subcluster Ih. In the present study, we applied a polyphasic approach by using cultivation-independent and culturing techniques in order to further characterize the occurrence, abundance, and physiological properties of subcluster Ih bacteria in low-sulfate, methanogenic environments. 16S rRNA (gene)-based cloning, quantitative fluorescence in situ hybridization, and real-time PCR analyses showed that the subcluster Ih population composed a considerable part of the Desulfotomaculum cluster I on November 11, 2015 by University of Queensland Library community in almost all samples examined. Additionally, five propionate-degrading syntrophic enrichments of subcluster Ih bacteria were successfully established, from one of which the new strain MGP was isolated in coculture with a hydrogenotrophic methanogen. None of the cultures analyzed, including previously described Pelotomaculum species and strain MGP, consumed sulfite, sulfate, or organosulfonates. In accordance with these phenotypic observations, a PCR-based screening for dsrAB (key genes of the sulfate respiration pathway encoding the alpha and beta subunits of the dissimilatory sulfite reductase) of all enrichments/(co)cultures was negative with one exception. Surprisingly, strain MGP contained dsrAB, which were transcribed in the presence and absence of sulfate. Based on these and previous findings, we hypothesize that members of Desulfotomacu- lum subcluster Ih have recently adopted a syntrophic lifestyle to thrive in low-sulfate, methanogenic environ- ments and thus have lost their ancestral ability for dissimilatory sulfate/sulfite reduction. Members of Desulfotomaculum cluster I have been generally treated taxonomically as an individual genus, all subcluster known as gram-positive, spore-forming, sulfate-reducing bac- members were until recently described as Desulfotomaculum teria (50, 56) and have frequently been found in various anoxic species due to the absence of sufficient distinguishing pheno- environments, such as sediments, rice paddy soil, human feces, typic and molecular features (50). However, the two recently and anaerobic sludges (for examples, see references 21, 42, 56, described species of the new genus Sporotomaculum lack the 57). The genus Desulfotomaculum includes over 20 validly de- ability to respire anaerobically with sulfate, although they scribed mesophilic and thermophilic species, all of which share are members of Desulfotomaculum subcluster Ib (3, 44). In the ability to oxidize various organic substances, like short- addition, Pelotomaculum thermopropionicum strain SI, rep- chain fatty acids, alcohols, and aromatic compounds with sul- resenting the novel subcluster Ih within Desulfotomaculum fate as a terminal electron acceptor (56). Due to these physi- cluster I (22, 23), is also lacking dissimilatory sulfate-reduc- ological traits, members of Desulfotomaculum cluster I have ing activity (22, 23). Importantly, strain SI grows syntrophi- been considered important in sulfidogenic, anoxic environ- cally with hydrogenotrophic methanogens (22, 23), whereas ments, where they play crucial roles in the degradation of only a few members of the genus Desulfotomaculum are able organic compounds, as well as in the biogeochemical cycling of to grow in syntrophic association with methanogens in the sulfur (56). absence of sulfate (26, 42). The collection of non-sulfate- On the basis of comparative 16S rRNA gene sequence anal- reducing bacteria belonging to Desulfotomaculum subcluster ysis, Desulfotomaculum cluster I was considered to be com- Ih was recently extended by the successful isolation of further prised of seven well-separated subclusters, Ia to Ig (27, 50, 52, syntrophic strains in coculture with hydrogenotrophic methano- 57). Although it has been argued that each subcluster could be gens: the propionate degrader Pelotomaculum schinkii (6, 7, 16) and the two phthalate-degrading strains JT and JI (42a, 43). Furthermore, Lueders et al. (37) reported that Pelotomaculum * Corresponding author. Mailing address: Department of Environ- spp. (i.e., subcluster Ih microbes) were one of the active in situ mental Systems Engineering, Nagaoka University of Technology, 1603-1 Kamitomioka, Nagaoka, Niigata 940-2188, Japan. Phone: 81-258-47-9642. syntrophic propionate-oxidizing populations in a rice field by Fax: 81-258-47-9642. E-mail: [email protected]. rRNA-based stable-isotope probing. 2080 VOL. 72, 2006 NON-SULFATE-REDUCING SYNTROPHIC DESULFOTOMACULUM CLUSTER I 2081 TABLE 1. Samples from methanogenic environments analyzed in this study Reactor Sulfate concn Influent Sample Sample operation Treating waste/wastewater in influent CODcra Location no. temp (°C) (mg/liter) (mg/liter) 1 Thermophilic digested sludge TJ 55 Municipal solid waste 20 93,550 Niigata, Japan 2 Thermophilic digested sludge TO 53 Municipal sewage sludge 56 59,000 Osaka, Japan 3 Thermophilic granular sludge TR2 55 Artificial wastewater 157 4,000 Our laboratory 4 Thermophilic granular sludge TD 55 Wastewater from clear liquor 149 12,000 Our laboratory manufacture Downloaded from 5 Mesophilic granular sludge MR1 35 Artificial wastewater 81 2,000 Our laboratory 6 Mesophilic granular sludge MB 35 Wastewater from beer factory 55 3,000 Ibaraki, Japan 7 Mesophilic granular sludge MC 35 Wastewater from sugar factory 58 1,635 Nara, Japan 8 Mesophilic digested sludge MD 35 Municipal sewage sludge 62 57,600 Niigata, Japan 9 Rice paddy soil RP Niigata, Japan a Chemical oxygen demand as determined using dichromate. http://aem.asm.org/ The degradation of organic matter by Desulfotomaculum Construction of 16S rRNA gene clone libraries. Extraction of DNA from cluster I bacteria in methanogenic environments has been anaerobic environmental samples and enrichment cultures was done according thought to be linked to dissimilatory sulfate reduction (21, 52). to a previously described protocol (38). Before PCR amplification, the extracted DNA was purified with a GENE CLEAN Turbo kit (BIO101, CA). Amplifica- Based on the results of this study and the previous studies tion of 16S rRNA genes was carried out according to the method in a previous mentioned above, we propose that subcluster Ih bacteria have study (48). The Desulfotomaculum cluster I-specific primer pair DEM116f/ adapted to anoxic, low-sulfate conditions and thus constitute a DEM1164r (52) and the universal bacterial primer pair 341F/1490R (40, 55) significant fraction of the Desulfotomaculum cluster I popula- were used for amplification of 16S rRNA genes from environmental samples and tion in methanogenic ecosystems. As a consequence of this enrichments, respectively (52). The PCR products were purified with a Micro- Spin Column (Amersham Biosciences) and subsequently cloned into E. coli using evolutionary process, they have lost the capability for sulfate the TA cloning kit (Novagen). Ten clones were randomly picked from each clone on November 11, 2015 by University of Queensland Library respiration and live in close proximity to hydrogen- and for- library for sequencing. 16S rRNA gene sequences with a sequence similarity of mate-consuming methanogens in order to maintain an ener- 100% were grouped into a “phylotype.” The name of each phylotype is composed getically favorable, low-hydrogen partial pressure for the syn- of the sample name and a number (for example, TJ-1 is clone number 1 recov- ered from the environmental sample TJ). trophic oxidation of organic substrates. PCR amplification of dsrAB and apsA. DNA extractions from pure (co)cul- tures (P. thermopropionicum, P. schinkii, S. fumaroxidans, and strains JT, JI, and MATERIALS AND METHODS MGP), as well as from enrichment cultures containing subcluster Ih bacteria, were performed according to the method of Hiraishi (20). The template quality Microorganisms and cultivation media. The following pure (co)cultures were of extracted DNA was tested by PCR with the 16S rRNA gene-specific primer used in this study. Pelotomaculum thermopropionicum strain SI was isolated in pair 341F (40) and 907R (28). PCR amplifications of the dsrAB and apsA genes our previous study (22, 23). Strain MGP was isolated in this
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