Microbial Community Dynamics during Composting Process of Animal Manure Analyzed by Molecular Biological Methods

著者 Yamamoto Nozomi, Asano Ryoki, Otawa Kenichi, Oishi Ryu, Yoshii Hiroki, Tada Chika, Nakai Yutaka journal or Journal of Integrated Field Science publication title volume 11 page range 27-34 year 2014-03 URL http://hdl.handle.net/10097/57385 lIFS, 11 : 27 - 34 (2014) Symposium Mini Paper (Oral Session)

Microbial Community Dynamics during Composting Process of Animal Manure Analyzed by Molecular Biological Methods

Nozomi Yamamoto!, RyokiAsano2, Kenichi Otawa3, Ryu Oishi3, Hiroki YoshiP, Chika Tada3 and Yutaka NakaP

IGraduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Japan, 2Department of Biotechnology, Faculty of Bioresource Sciences, Akita Prefectural University, Japan, 3Graduate School of Agricultural Science, Tohoku University, Japan

Keywords: 16S rRNA gene, animal manure, archaea, bacteria, cloning, compost

Abstract we revealed the pattern of changes in the prokaryotic Composting is a biological process involving sta­ communities involved in the compo sting process. bilization of animal manure and transformation into organic fertilizer. Microorganisms such as bacteria Introduction and archaea participate in the compo sting process. Cattle manure accounts for a large part of the total Because bacteria form huge communities in compost, animal waste generated in Japan (MAFF, 2013) and they are thought to play an important role as decom­ can cause environmental problems such as soil con­ posers of organic substances. However, only few tamination, air pollution, or offensive odor emission studies are tracking bacterial communities throughout without appropriate treatment (Bernal et aI., 2008). the composting process. The role of archaeal com­ Composting is the most effective technique for min­ munities in compo sting has not been also elucidated. eralization of organic substances, microbial stabiliza­ To study bacterial and archaeal community dynamics, tion, removal of odors, and sanitization (Bernal et aI., animal manure composts were analyzed by molecular 2008; Haga, 1999). In addition, the final product can biological methods. be applied to agricultural soil as high quality fertil­ A clone library constructed from bacterial 16S izer (Haga, 1999). Throughout the process, various rRNA genes showed that the bacterial community microorganisms such as bacteria, archae a, and fungi structure dynamically changed with processing time. play an important role in degradation (Ryckeboer et Based on phylum-level analysis, Firmicutes and Bac­ aI., 2003). Microbial community structure and diver­ teroidetes were dominant at day o. Phylum Firmicutes sity change dramatically during composting. These kept their abundance for 20 days, indicating that they changes are affected by temperature, pH, moisture may be active under high temperatures. In the final content, and aerobic/anaerobic conditions (Ryckeboer compost, the library consisted of various genes be­ et aI., 2003; Schloss et aI., 2003). Because the bacte­ longing to the phyla Proteobacteria, Bacteroidetes, rial population is more vast and complex than others Firmicutes, and Actinobacteria. (Ryckeboer et aI., 2003), it has been considered that In contrast, the clone library of archaeal 16S rRNA the bacterial community is the main decomposer in genes was simply constructed by two groups, the compost. To follow the dramatic change in structure methane-producing archaea (methanogens) and and diversity of the microbial community during ammonia-oxidizing archae a (AOA). Thermophilic composting, researchers have recently used culture­ Methanosarcina spp.-like genes were constantly independent techniques analyzing 16S ribosomal present, indicating that this methanogen may adapt RNA genes (Chachkhiani et aI., 2004; Peters et aI., to environmental changes such as high temperature. 2000; Tang et aI., 2004). Using culture-dependent AOA-like sequences were first detected from com­ techniques, it is possible to detect only about 8.5% of post and displayed a high similarity to cultured AOA total microbes (Gong et aI., 2005). The changes in the originating from hot springs. Further study revealed bacterial community structure during the compo sting that the abundance of AOA markedly varied because of animal manure have been analyzed in other stud­ of raw material or compo sting process. In this study, ies (Cho et aI., 2008; Green et aI., 2004; Maeda et aI.,

27 Yamamoto, N. et al.

2010; Sasaki et aI., 2009; Yamamoto et aI., 2009); cal and chemical parameters are shown in Fig. 1. however, there are only few studies tracking the bac­ The temperature reached 76.1 °C within 5 days and terial community in detail throughout the entire com­ remained at >50 °C for 23 days. Moisture content de­ posting process. On the other hand, existing studies of creased from about 70% to 41.8 % by the end of the the archaeal community are a minor component of the process (Fig. 1). microbial community studies on composting because We selected 5 samples at different time points for archaea mainly live in extreme environments such as analysis. Total DNA was extracted and approximately thermophilic or anaerobic conditions (lnsam and de 600 bp of bacterial 16S rRNA gene were amplified. Bertoldi, 2007). However, some reports have indicat­ PCR products with the correct DNA fragments were ed the presence of methane-producing archaea (meth­ cloned and then selected for sequencing. anogens) in compost (Jackel et aI., 2005; Thummes The clone library constructed from the sample col­ et aI. , 2007). Moreover, a new archaeal group called lected on day 0 mainly consisted of members of the ammonia-oxidizing archae a (AOA) was discovered phyla Firmicutes and Bacteroidetes (Fig. 2), indicat­ living in moderate environments like seawater and ing that both members of bacteria originating from soil and were found to be essential organisms in am­ cattle manure (Ozutsumi et aI. , 2005). The number of monia oxidation (Konneke et aI. , 2005; Leininger et clones grouped under the phylum Firmicutes, which aI., 2006; Treusch et aI. , 2005). Therefore, archaea can be active under high temperatures, maintained can be also considered as an essential component of their relative abundance for 20 days. Especially on the microbial community in compost. However, there day 5 and day 20, the Phylum consists of the member is no existing study of the entire archaeal community of class Clostridiales and Bacillales, corresponding in the compo sting of animal manure. to other reports (Yamada et aI. , 2008). Thereafter, In this review, we investigated the bacterial and archaeal community structures and how they changed during the compo sting process. 80 100

70 90 80 Bacterial community structure during the com­ 60 70 posting process 50 G 60 C ~ It has been considered that bacteria play an impor­ 40 50 c ~ Co ~ B Co c tant role throughout the process because of the exis­ 6 40 8 ~ 30 .. =- --Temperature 30 .. tence of a wide variety of species and characteristics. E! 01 20 ~ ~ 20 A Water content Denaturant gradient gel electrophoresis (DGGE) has 10 10 been widely used for the analysis of bacterial com­ 0 0 munities (Green et aI. , 2004; Maeda et aI. , 2010; Sa­ 14 28 42 56 70 84 98 11 2 Composting days saki et aI. , 2009; Yamamoto et aI. , 2009). However, it is not sufficient to clarify the change in the dominant Fig. 1. Changes in temperature and water content during the compo sting process for analysis of microbial species in bacterial communities during the bacterial community. composting process. The clone library method en­ ables detection of a larger number of species within microbial communities than using DGGE analysis. 100

However, only few studies are tracking bacterial ~ 80 o Unclassified ra other C communities throughout the composting process "o • ctinobacteria ~ 60 (Cho et aI. , 2008; Guo et aI. , 2007; Yamada et aI. , C Mollicutes

j o Gammaprotcobacleria 2008). Here, we performed a composting experiment 40 ~ o Betaproteobacteria as a model case of field-scale compo sting and tracked "> L'9 Alphaproteobactcria .~ 20 • Finnicutes the bacterial community using the cloning procedure. ~ - Bacteroidetcs Cattle manure and sawdust were mixed and piled for about 30 days with aeration. To study the bacterial Day 0 Day 5 Day 20 Day 28 Day 112 community, composting material was treated for 84 Age of compost days more without daily mixing. Changes in physi- Fig. 2. Changes in bacterial community constructed from cloned 16S rRNA genes.

28 Microbial Community Dynamics during Composting Process of Animal Manure Analyzed by Molecular Biological Methods the ratio of the members of the phylum Firmicutes was available, although methanogen-like sequences decreased, while those of the phyla Actinobacte­ had been detected in cattle manure (Gattinger et ai. ria and Proteobacteria increased. By the end of the 2007). Thummes et aI. (2007) analyzed about 120 composting process, the library consisted of phyla clone sequences using composting materials; how­ Proteobacteria (32.7%), Bacteroidetes (26.5%), Fir­ ever, no sequence belonging to AOA was detected. micutes (18.4%) and Actinobacteria (12.2%), and Therefore, the compo sting experiment to analyze others (l0.2%), showing that various bacteria lived the archaeal community was performed using cattle and forms complex community in the final compost. manure and sawdust as described above (Yamamoto Bacteria sequences were classified into class Rhizo­ et aI. , 2011). Changes in physical and chemical biales and Burkholderiales, that often observed in parameters are shown in Fig. 1. The temperature soil environment were also contained, suggesting that reached 77.9°C and was maintained at >60°C for 18 compo sting material reached stable phase. days. The initial moisture content was about 67% We observed that the bacterial community reflected (Fig. 3), and it continued to decline from day 8 and compo sting conditions and changed its structure ac­ eventually reached its lowest value (~30%). cordingly. However, metabolic activity of bacterial Compost samples for analysis were selected at 6 community was not analyzed in this study. To deter­ time points. In total, 14 OTUs were generated from mine dominant species in each stage of the compost­ sequenced clones, the number of which varied from ing process, RNA-based analysis is required. Some 36 to 78 . Almost all detected OTUs were related studies reported the community structure of one either to methanogens or to AOA (Fig. 4). Results particular bacterial group diversity in compost with indicated that both methanogens and AOA were reverse-transcription PCR and DGGE (Halet et aI. , dominant archaeal species during the composting 2006; Kowalchuk et aI. , 1999). In addition, metage­ process of cattle manure. The archaeal community nomic analysis may be also the powerfull method for understanding whole microbial community in com­ 80 100 post (Martins et ai. 2013). It will cover all aspects of 70 80 -. microbial ecology in composting in combination with 0'60 ~ 0 ~ PCR-based DNA analysis. 'E' 50 1: 60 ~ = 1: ~ 40 Q C.I ~ 40 ... Archaeal community structure during the com­ e30 ...~ posting process ~ 20 ~ 20 It has long been considered that the archaeal com­ 10 t:, Water content munity has a low abundance in composting process 0 0 because they are usually oligotrophic, thermophilic, 0 5 10 15 20 25 30 or hyperthermophilic (Insam and de Bertoldi, 2007). Composting days However, the archaeal community has recently been considered as an essential component of the micro­ Fig. 3. Changes in temperature and water content during the compo sting process for analysis of bial community in compost. For instance, consider­ archaeal community. able methane emissions have been measured from compost, suggesting that methane-producing archaea 100 -r-- - (methanogens) live actively in compost (Beck-Friis et e. o Methanosarcina spp. '"Q) aI. , 2000; Fukumoto et aI. , 2003 ; Hao et aI. , 2001). In I'l 80 r-- r-- r-- r-- - • Methanocorpusculum spp. ~ m Other methanogcn addition, some archaea of the phylum Crenarchaeota ~ 60 r-- I-- I-- I-- r-- Q) • Candidatus Nitrososphaera spp. l:!as can oxidize ammonia under natural environments "C -- o Other Crenarchaeota I'l 40 r-- I-- r-- ::s I!l Other Euryarchaeota such as seawater, freshwater, various soil, and hot ..0as Q) 20 r-- I-- -- r-- spring (Hatzenpichler et aI. , 2008; Konneke et aI. , .~ .!! ~ 2005; Leininger et aI., 2006; Treusch et aI. , 2005). Day 0 Day 2 Day 6 Day 16 Day 24 Day 30 AOA also was detected from artificial sites, like rice Age of compost field (Fujii et aI. , 2010). However, no useful informa­ tion about archaea in the compost of cattle manure Fig. 4. Changes in archaeal community constructed from cloned 16S rRNA genes.

29 Yamamoto, N. et al.

structure found in the present study differed in some moto et aI., 2010). In the samples collected from cat­ respects from that found in previous reports analyz­ tle manure compost, only one or two archaeal amoA ing composting materials. During the first two days, bands were detected in the course of the composting OTU s grouped into methanogens were dominant. process (Yamamoto et aI., 2011). It was shown a use­ We detected some OTUs, which were closely related ful information that the diversity of AOA community with sequences from groundwater, animal rumen, or was low and AOA may have an ability of ammonia manure. oxidation in composting. In addition, our group also Another OTU formed the dominant group after revealed that an archaeon related to Candidatus day 2 and showed a high homology with uncultured Nitrososphaera gargensis was dominant in liquid thermophilic Methanosarcina spp. Thummes et ai. cultures seeded with cattle manure compost (Oishi (2007) also detected some clones grouped into this et aI., 2012). However, there is no information avail­ cluster from different composting materials. Thus, able about AOA communities in other animal ma­ thermophilic Methanosarcina-like organisms appear nure compost. To clearly understand the nitrification to adapt to the compo sting environment and increase process in compost ecosystems, we researched AOA its detection rate after other methanogens originating community structure in various animal composts (Ya­ from cattle manure have decreased in abundance be­ mamoto et aI., 2012). For AOA community analysis, cause of high temperatures. the bacterial amoA sequence was also amplified to It is notable that AOA-like sequences were de­ compare their diversity and abundances. tected throughout the composting process. Our study Samples collected from other cattle manure com­ indicated that AOA was an essential component of post were also able to amplify archaeal amoA se­ the archaeal community in compost, particularly quences and show DGGE fingerprints. In contrast, a from days 6 to 30. A large part of OTU was closely few amoA sequences were amplified using samples related to Candidatus Nitrososphaera gargensis with from fresh manure, swine manure compost, and high homology (98%). This Candidatus Nitrosos­ chicken manure compost. The number of detected phaera gargensis-like AOA can grow under moder­ amoA sequences per sample varied from 1 to 4, ex­ ate thermophilic condition and may have the ability cept for the samples from one facility. All sequences to oxidize ammonia to nitrite (Hatzenpichler et aI., were divided into about three groups: one is phy­ 2008). The AOA detected in the sample adapted to logenetically related to Candidatus Nitrososphaera the temperature or ammonium concentration in cattle gargensis (group NG), while the other two groups manure compost. Other OTU s were classified as soil had amoA sequences from hot spring or wastewater crenarchaeota. as close relatives (Fig. 5). However, there were a few compost samples where AOA dominated over AOBs, Diversity of ADA in various animal manure indicating that the presence and abundance of ammo­ composts nia oxidizers was determined by some unknown fac­ Nitrification by ammonia oxidation occurs during tors. We hypothesized that the difference of ammonia composting process (Bernal et aI., 2009; Vuorinen concentration between raw animal manure is the most and Saharinen, 1997). Organic nitrogen in fresh ma­ influential factor in AOA presence and cattle manure nure is oxidized to nitrate through nitrification by was the best material to their growth in composting. ammonia oxidizing organisms. It has been reported that ammonia-oxidizing bacteria (AOB) may play The number of AOA cells in comparison to am­ an important role in nitrification during composting monia-oxidizing bacteria (AOB) in the sample was (Prosser and Nicol, 2008). However, previous re­ estimated by real-time PCR (Fig. 6). In cattle manure searchers concluded that archaeal amoA gene was not compost, the abundance of archaeal amoA genes was detected from any stages of the composting process clearly lower than that of bacterial genes. These re­ (Maeda et aI., 2010; Yamada et aI., 2007). Our study sults provided the finding that the abundance of AOA detected the archaeal amoA gene in compost for the in compost was not influenced by the difference of first time (Yamamoto et aI., 2010). It shows thatAOA animal species generating manure. Real-time PCR may have been more abundant than AOB during the confirmed that archaeal amoA gene copy numbers cooling and maturation stages of composting (Yama- were greater than bacterial gene copy numbers in the

30 Microbial Community Dynamics during Composting Process of Animal Manure Analyzed by Molecular Biological Methods

AOA Ah e (A8688005) 61 AOA=Ch=c (AB688018) 66 P2_2 (HM803767) 84 AOA_Ah_f(A8688006) AOA_Ah_B (AB688001) ,----:-=-1>1 AOA_Ah_b (A8688002) AOA_Ah_c (A8688003) AOA_Af_c (A8688010) 100 82 UAS 020 C.01 64(A B353450) lOa AOA.=Ah_d (AB688004) S-47 (I 1M 345999) lOa AOA_Ch_c (AB688020) KHLamoAp3-3 (HM467064) AOA_Ch_b (AB688017) 74 100 AOA_ACb (AB688009) BJ-30-11 (FJ940170) AOA_Dh_B (AB688023) AOA_CCB (AB688021) DGGE band: K09_a (AB542171) AOA_Hh_B (A8688027) '------"70d AOA_Ch_B (AB688016) 87 10O AOA_ACB (AB688008) AOA_HCa (AB688028) AOA_Bh_a (AB688012) 100 AOA_Dh_d (AB688026) ,------'-""'1 BGA-545 (EU590l83) '-----Nitrososphaera liennensis (FR773159) ,..------Candidatus Nitrososphaera gargensis (EU2l! 1318) 100 100 AOA_Jh_B (A8688029) Ice15B (EU414220) 87 AOA_Jh_b (AB688030) RW-4 (AB525380) 93 AOA_Dh_b (AB688024) AOA_Bh_b (A8688013) AOA_8h_c (A8688014) 96 AOA_Ch_d (A8688019) AOA_Ah~ (AB688007) group NG 96 AOA_Af_d (AB688011) AOA_Dh_c (A8688025) AOA_Cf_b (A8688022) 63 AOA_Bf_a (AB688015) 65 DGGE band: K09_b (AB542 172) ,..------Candidatus Nitrosocaldus yellowstonii (EU239961) '------Nilrosopumilus maritimus (EU239959)

0.05

Fig. 5. Phylogenetic tree of the archaeal amoA sequences obtained from compo sting materials.

109 ~ .AOA ~ lOS DAOB ~ 0.. 0 u 7 c:(1) 10 (1) OJ) ""'l::: 6 C 10 1::: ~ 4.- ...0 105 (1) ..D E ;:l 4 Z 10 103 eo eo .0 t tot t tt t t t t to t t tt tt tt tt hfhfhfmhfmhfmhfmhfmhfmhfhf A Be DE F G HI J (cattle) (cattle and swine) (swine) (chicken) Sampling site (manure type) Fig. 6. AmoA gene copy numbers for AOA and AOB. Capi­ tal letter indicates sampling facilities. Samples were obtained from each facility at fresh manure (m), the high temperature stage (h), and the end of the com­ posting (t). Samples with dagger did not perform real-time PCR. The sample with gene copy number below the detection limit were represented as closed circle (AOA) and opened circle (AOB).

31 Yamamoto, N. et al.

end product at facility H. The AOAIAOB ratios var­ teria for compost maturity assessment. A review. ied from 0.06 to 10.54. This variation may have been Bioresource Technology, 100: 5444-5453 caused by the operating conditions of the compo sting Cahyani, V. R., K. Matsuya, S. Asakawa, and M. process, such as the addition of finished compost. Kimura (2004) Succession and phylogenetic pro­ Our results so far suggest that the concentration file of methanogenic archaeal communities during of ammonium and the temperature are factors that the composting process of rice straw estimated by control the AOA community. Further study is needed PCR-DGGE. Soil Science and Plant Nutrition, 50: to show whether AOA are critical to nitrification in 555-563 manure compost and influence the quality of the com­ Cho, K., S. Lee, R. Math, S. Islam, D. Kambiranda, J. post. To evaluate the contribution of AOA in nitrifica­ Kim et al. (2008) Culture-independent analysis of tion, we need to collect and analyze more compo sting microbial succession during compo sting of Swine samples and measure various parameters to create slurry and mushroom cultural wastes. Journal of meta-data for future research. Microbiology & Biotechnology, 18: 1874-1883 Fujii, C., T. Nakagawa, Y. Onodera, N. Matsutani, Conclusion K. Sasada, R. Takahashi, and T. Tokuyama (2010) In this study, we revealed a part of the pattern of the Succession and community composition of ammo­ changes in the bacterial community in the compost­ nia-oxidizing archaea and bacteria in bulk soil of a ing process by analyzing a large number of bacterial Japanese paddy field. Soil Science and Plant Nutri­ sequences. In addition, we detected AOA from com­ tion, 56: 212-219 post for the first time. By studying various samples Fukumoto, Y., T. Osada, D. Hanajima, and K. Haga

, originating from different animal manure samples, we (2003) Patterns and quantities of NH3 N20 and were also able to suggest that AOA could be involved CH4 emissions during swine manure composting in the nitrification of composting systems, although without forced aeration-effect of compost pile their abundance was lesser than that of AOBs. This scale. Bioresource Technology, 89: 109-114 study underlines the importance of investigating ar­ Gattinger, A., M.G. Hofle, M. Schloter, A. Embacher, chaeal communities to understand the microbiology F. Bohme, J.C. Munch, and M. Labrenz (2007) of compost. Traditional cattle manure application determines However, metabolic activity of bacterial and ar­ abundance, diversity and activity of methanogenic chaeal community were not analyzed in this study. Archaea in arable European soil. Environmental RNA-based analysis and metagenomics will cover all Microbiology, 9: 612-24 aspects of microbial ecology in compo sting by com­ Gong, C.H., J. Koshida, K. Inoue, and T. Someya bining with PeR-based DNA analysis. (2005) Fluorescence direct count of bacteria in various manures and composts as compared with Acknowledgements plate count. Jpn Journal of Soil Science and Plant This work was supported, in part, by the F ounda­ Nutrition, 76: 401-410 [in Japanese] tion of the Ministry of Education, Culture, Sports, Green, S., F.J. Michel, Y. Hadar, and D. Minz (2004) Science and Technology, Japan, as a "Project of In­ Similarity of bacterial communities in sawdust­ tegrated Compost Science" and by a grant from the and straw-amended cow manure composts. FEMS Livestock Technology Association, Japan. Microbiology Letters, 233: 115-123 Guo, Y., N. Zhu, S. Zhu, and C. Deng (2007) Mo­ References lecular phylogenetic diversity of bacteria and its spatial distribution in composts. Journal of Applied Beck-Friis, B., M. Pell, U. Sonesson, H. Jonsson, and Microbiology, 103: 1344-1354 H. Kirchmann (2000) Formation and emmission Haga, K (1999) Development of composting technol­

of N20 and CH4 from compost heaps of organic ogy in animal waste treatment. Asian-Aus Journal household waste. Environmental Monitoring and of Animal Science, 12: 604-606 Assessment, 62: 317-331 Halet, D., N. Boon, and W. Verstraete (2006) Com­ Bernal, M.P., lA. Alburquerque, and R. Moral (2009) munity dynamics of methanotrophic bacteria dur­ Composting of animal manures and chemical cri- ing compo sting of organic matter. Journal of Bio-

32 Microbial Community Dynamics during Composting Process of Animal Manure Analyzed by Molecular Biological Methods

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