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Comparative Analysis of Bacterial and Archaeal Communities In Microbes Environ. Vol. 24, No. 2, 88–96, 2009 http://wwwsoc.nii.ac.jp/jsme2/ doi:10.1264/jsme2.ME08561 Comparative Analysis of Bacterial and Archaeal Communities in Methanogenic Sludge Granules from Upflow Anaerobic Sludge Blanket Reactors Treating Various Food-Processing, High-Strength Organic Wastewaters TAKASHI NARIHIRO1, TAKESHI TERADA1,2, KAE KIKUCHI2, AKINORI IGUCHI1, MIZUYO IKEDA2, TOSHIHIRO YAMAUCHI2, KOJI SHIRAISHI2, YOICHI KAMAGATA1,3, KAZUNORI NAKAMURA1, and YUJI SEKIGUCHI1* 1Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science and Technology (AIST), 1-1-1 Higashi, Tsukuba, Ibaraki 305-8566, Japan; 2Fujikasui Engineering Co., Ltd., 1-4-3 Higashi-gotanda, Shinagawa, Tokyo 141-0022, Japan; and 3Research Institute of Genome-based Biofactory, National Institute of Advanced Industrial Science and Technology (AIST), 2-17-2-1 Tsukisamu-Higashi, Toyohiraku, Sapporo, Hokkaido 062-8517, Japan (Received December 1, 2008—Accepted February 9, 2009—Published online March 13, 2009) A comprehensive survey of bacterial and archaeal community structures within granular sludges taken from twelve different types of full-scale, food-processing wastewater-treating, upflow anaerobic sludge blanket (UASB) reactors was performed with a 16S rRNA gene-based clone library method. In total, 1,282 bacterial 16S rRNA gene clones and 722 archaeal clones were analyzed, and their identities were determined by phylogenetic analyses. Overall, clones belonging to the bacterial phyla Proteobacteria (the class Deltaproteobacteria in particular), Firmicutes, Spirochaetes, and Bacteroidetes were observed in abundance within the bacterial clone libraries examined, indicating common bacte- rial denominators in such treatment systems. Within the domain Archaea, clones affiliated with the classes Methano- microbia and Methanobacteria were found to be abundant in the archaeal libraries. In relation to features of reactor performance (such as chemical oxygen demand removal, fatty acid accumulation, and sludge bulking), possible representative phylotypes likely to be associated with process failures, such as sludge bulking and the accumulation of propionate, were found in comparative analyses of the distribution of phylotypes in the sludge libraries. Key words: 16S rRNA gene clone library, granular sludge, microbial community, UASB Anaerobic digestion technology has been used effectively yses have been performed for UASB granular sludges treat- to treat organic matter in waste streams. To date, various ing wastewater from a paper factory (41), a terephthalate- anaerobic processes for treating wastewater have been devel- manufacturing plant (53), a beer brewery (13), and sucrose/ oped (1, 29, 32). One of the most established technologies in propionate/acetate-based artificial wastewater (44). In addi- this field is the upflow anaerobic sludge blanket (UASB) sys- tion, the molecular characterization of UASB granules tar- tem, because of its ability to treat a broad range of organic geting specific microbial groups has also been reported (10, waste streams at high loading rates (32, 40, 45, 47). The most 20, 31). According to these studies, the 16S rRNA gene characteristic phenomenon in this process is sludge granula- clones retrieved from UASB sludges indicated the major tion, i.e., granular-shaped sludge is spontaneously formed microbial constituents to be those of the phyla Proteobacte- within the system. Granular sludge generally has superior ria, Chloroflexi, Firmicutes, Spirochaetes, and Bacteroidetes settling characteristics. Thus, the stable and efficient opera- in the domain Bacteria, and those of the classes Methano- tion of granular sludge-based systems is primarily dependent microbia, Methanobacteria, and Thermoplasmata in the on the growth and maintenance of granular sludge. Granular domain Archaea (47). In addition, such studies have also sludge is also characterized as a spherical biofilm, possessing shown that a large number of the clones assigned to candi- all the trophic groups of anaerobes necessary for the com- date phyla (known as ‘clone clusters’) were frequently found plete mineralization of organic matter. Owing to its charac- in such ecosystems (7, 8, 10, 20, 31, 48, 55). However, there teristic internal structure, granular sludge is also important are still obstacles to precisely determining and monitoring for the efficient biotransformation of organic matter into the entire microbial community of sludge because of the lim- methane (48). ited number of datasets reported so far. Understanding the ecology of anaerobes involved in gran- To create more complete microbial biodiversity maps in ular sludge is essential to the control of these bioreactors. relation to reactor performance and wastewater type, it is The microbiology of granular sludges in UASB bioreactors necessary to further increase the biodiversity data of UASB has been studied using culture-dependent and molecular- sludge granules in association with data on process failures. based approaches, particularly those targeting 16S rRNA In the present study, we attempted the exhaustive character- genes (38, 45, 47). So far, molecular-based community anal- ization of methanogenic granular sludge in full-scale UASB reactors treating various types of food-processing, high- * Corresponding author. E-mail: [email protected]; Tel: +81– strength organic wastewater. Since a more extensive applica- 29–861–7866; Fax: +81–29–861–6400. tion of UASB technology is still hampered by concerns over Microbial Community in UASB Sludges 89 operational instability such as the accumulation of volatile 16S rRNA gene clone library fatty acids (14, 24), formation of scum (23, 50), and sludge Bacterial and archaeal 16S rRNA gene clone libraries were con- bulking (3, 15, 46, 55), special attention was paid to UASB structed for all the samples listed in Table 1. DNA extraction and bioreactors associated with volatile fatty acid accumulation PCR amplification were performed as described previously with and sludge bulking in choosing representative bioprocesses. slight modifications (37, 39, 54). The partial 16S rRNA genes were amplified with the primer set EUB338mix (5'-ACWCCTACGGG- Comparative analyses of bacterial and archaeal 16S rRNA WGGCWGC-3'), which consists of an equal amount (mol) of gene clone inventories of 12 granular sludges were per- EUB338 (2), EUB338II (12), and EUB338III (12) forward primers formed, and the phylogenetic identities of the major and (possessing sequences complementary to those of the EUB338 characteristic phylotypes were determined. probe set, Escherichia coli position 338–355), and the reverse primer UNIV1492r (5'-TACGGYTACCTTGTTACGACTT-3', E. Materials and Methods coli position 1492–1513) (30) for the domain Bacteria, and ARC109f (5'-ACKGCTCAGTAACACGT-3', E. coli position 109– UASB process 125) (22) and UNIV1492r for the domain Archaea. The thermal cycle profile consisted of preheating at 95°C for 9 min and 20 UASB sludge samples were taken from 12 full-scale UASB reac- cycles of denaturation at 95°C for 30 s, annealing at 50°C for 30 s, tors that treat various types of food-processing wastewater (Table and extension at 72°C for 2 min; the final step was followed by post 1). Based on wastewater type, the reactors are categorized into extension for 10 min. PCR products were purified with a QIAquick seven groups, namely (i) isomerized sugar-processing, (ii) sugar- PCR Purification Kit (Qiagen, Valencia, CA, USA), and subcloned based food-processing, (iii) vinegar-processing, (iv) soybean-based with a TA cloning kit (Novagen, Madison, WI, USA) according to product-processing, (v) salted vegetable-processing, (vi) alcohol- the manufacturer’s instructions. Cloned 16S rRNA genes were processing, and (vii) amino-acid-processing wastewater treatments sequenced with a Quick start kit (Beckman Coulter, Fullerton, CA, (Table 1). Groups (i) and (ii) are those for the treatment of organic USA) and a CEQ 2000XL automated sequence analyzer (Beckman wastewaters discharged from production lines of isomerized sugar, Coulter). Approximately 100 bacterial and 50 archaeal gene clones and from food production lines using sugars. Group (iii) is for were randomly retrieved from each granular sludge sample. wastewater from vinegar production lines. Group (iv) is for waste- Sequence data (ca. 500 bp) were imported into the ARB program waters discharged from food production lines using soybean, such package (33) and aligned using the editing tool in the program. as those for soy source production. Group (v) is for wastewater Phylotype was defined as a group of cloned sequences with from the production of vegetables pickled in salt. Group (vi) is for >97.0% identity. For the phylotypes that are comprised of more wastewater from the production lines of alcohol (clear liquor), and than three clones, nearly full-length 16S rRNA gene sequences (ca. group (vii) is for wastewater of the production lines of artificial sea- 1,100 bp for the domain Bacteria, and ca. 1,400 bp for the domain sonings. All of these processes were located in Japan and operated under mesophilic conditions (35–40°C). The reactors N1 and N2 Archaea) were determined. Construction and sequencing of archaeal were treating identical wastewater discharged from the same sugar- 16S rRNA gene clone libraries for the reactors Sw and Dt (49 processing manufactory in parallel. Chemical oxygen demand clones for the Sw reactor and 72 clones for the Dt reactor) were (COD) was analyzed by the standard
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