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In Situ Identification of Keratinhydrolyzing Organisms In RESEARCH ARTICLE In situ identification of keratin-hydrolyzing organisms in swine manure inoculated anaerobic digesters Yun Xia1, Daniel I. Masse´ 1, Tim A. McAllister2, Carole Beaulieu3, Guylaine Talbot1, Yunhong Kong2 & Robert Seviour4 1Dairy and Swine Research and Development Centre, Agriculture and Agri-Food Canada, Sherbrooke, QC, Canada; 2Lethbridge Research Centre, Agriculture and Agri-Food Canada, Lethbridge, AB, Canada; 3De´ partement de biologie, Universite´ de Sherbrooke, Sherbrooke, QC, Canada; and 4Biotechnology Research Centre, La Trobe University, Bendigo, Vic., Australia Downloaded from https://academic.oup.com/femsec/article/78/3/451/600873 by guest on 23 September 2021 Correspondence: Daniel I. Masse´ , Dairy and Abstract Swine Research and Development Centre, Agriculture and Agri-Food Canada, 2000 Feathers, a poultry byproduct, are composed of > 90% keratin which is resis- College Street, Sherbrooke, QC, Canada, tant to degradation during anaerobic digestion. In this study, four 42-L anaero- J1M 0C8. Tel.: +1 819 565 9171; fax: +1 bic digesters inoculated with adapted swine manure were used to investigate 819 564 5507; e-mail: daniel. [email protected] feather digestion. Ground feathers were added into two anaerobic digesters for biogas production, whereas another two without feathers were used as negative Received 10 February 2011; revised 9 May control. Feather degradation and enhanced methane production were recorded. 2011; accepted 21 July 2011. Final version published online 15 September Keratin-hydrolyzing organisms (KHOs) were visualized in the feather bag fluids 2011. after boron-dipyrromethene (BODIPY) fluorescence casein staining. Their abundances correlated (R2 = 0.96) to feather digestion rates. A 16S rRNA clone DOI: 10.1111/j.1574-6941.2011.01188.x library was constructed for the bacterial populations attached to the feather particles. Ninety-three clones (> 1300 bp) were retrieved and 57 (61%) Editor: Alfons Stams belonged to class Clostridia in the phylum Firmicutes, while 34 (37%) belonged to class Bacteroidia in the phylum Bacteroidetes. Four oligonucleotide FISH Keywords probes were designed for the major Clostridia clusters and used with other anaerobic digesters; keratin-hydrolyzing FISH probes to identify the KHOs. Probe FIMs1029 hybridized with most organisms; BODIPY FL protease staining; > fluorescence in situ hybridization; full-cycle ( 80%) of the KHOs. Its targeted sequence perfectly matches that possessed rRNA approach. by 10 Clostridia 16S rRNA gene clones belonging to a previously uncharacter- ized new genus closely related to Alkaliphilus in the subfamily Clostridiaceae 2 of family Clostridiaceae. biotechnologically more attractive alternatives. For exam- Introduction ple, feathers have been recycled after cooking under high Feathers are a poultry byproduct composed of > 90% pressure and temperature to make a feather meal suitable keratin (Astbury & Beighton, 1961), mostly as b-keratin for use as an animal protein supplement (Odetallah et al., (Sawyer et al., 2000). b-keratin is recalcitrant to degra- 2003) or as a slow-releasing nitrogen fertilizer (Choi & dation by many proteases because of the presence of Nelson, 1996). However, hydrothermal treatment of extensive disulfide bonds and cross-linkages (Papado- feather keratin is expensive and destroys several valuable poulos et al., 1986). Because feathers are generated in amino acids. The resulting product is poor in digestibility millions of tons annually, their disposal is an important and has a variable nutrient quality (Wang & Parsons, part of solid waste management (Onifade et al., 1998). 1997). Traditionally, feathers are treated as an organic solid Feathers have been used in anaerobic digestion systems waste, being incinerated or disposed at waste disposal to produce methane biogas but are poorly degraded MICROBIOLOGY ECOLOGY MICROBIOLOGY sites. These treatments are wasteful because feather kera- under anaerobic conditions (Salminen & Rintala, 2002). tin is rich in useful amino acids and its disposal by such Pretreatments including thermal, chemical, and enzymatic methods generates greenhouse gases (Salminen & Rintala, methods have been used in attempts to increase their 2002). Consequently, efforts have been made to develop digestion rates (Onifade et al., 1998). When Williams & FEMS Microbiol Ecol 78 (2011) 451–462 ª 2011 Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada Published by Blackwell Publishing Ltd. 452 Y. Xia et al. Shih (1989) enriched a mixture of bacteria using ball- bags and washed (delicate cycle) in a washing machine milled feather agar, the resultant bacterial community (Frigidaire, Martinez, GA) with tap water. Feather sam- showed keratinase activity capable of degrading auto- ples were then dried at 45 °C in a Unithern dryer (Con- claved whole feathers. Feather degradation has been struction CQLTD, England) until a constant weight was reported in anaerobic digesters (ADs) treating poultry reached (after about 8 weeks). The samples were ground waste including manure and/or mixed fractions of bone, through a 4-mm screen (Thomas-Wiley Laboratory Mill) trimmings and offal under thermophilic (Williams & and divided into portions of 33 g each and placed in Shih, 1989) or mesophilic (Salminen & Rintala, 2002) nitrogen-free polyester bags with a pore size of 50 lm condition. However, the chemical transformation and the (ANKOM Technology, Macedon, NY). Each bag was organisms responsible for this degradation have not been sealed with a plastic tie wrap and washed in the washing characterized in detail. machine to remove any remaining residual particles with Downloaded from https://academic.oup.com/femsec/article/78/3/451/600873 by guest on 23 September 2021 Keratin-hydrolyzing bacteria and keratinase enzyme a diameter < 50 lm. Finally, the bags were dried at 45 °C mixtures have also been reported to digest prions respon- until a constant weight ( 31 g each) was achieved. As sible for transmissible spongiform encephalopathies or required, 14 bags were then attached onto a steel stick prion diseases including bovine spongiform encephalopa- and inserted into an AD. thy (BSE), sheep scrapie, deer chronic waste disease, and human Creutzfeldt-Jakob disease (Gupta & Ramnani, Anaerobic digester set up 2006). Keratinases secreted by thermophilic bacterial strains VC13, VC15, S290 and Streptomyces sp. S6 (Tsi- Four 42-L Plexiglas ADs and one 7-m3 semi-industrial roulnikov et al., 2004), Bacillus licheniformis strain PWD-1 AD, as described by Masse´ et al. (2001), were used in this (Langeveld et al., 2003) and Bacillus MSK103 (Yoshioka study. The 7-m3 semi-industrial AD was used to adapt et al., 2007) were shown to inactivate prions, because the fresh swine manure collected from a commercial pig farm structures of prions and feather keratin share many char- (Sherbrooke, Quebec) that processes about 4000 pigs per acteristics. Both are fibrous and insoluble proteins rich in year, which was then used to inoculate (representing b-sheet (Fraser et al., 1972). BSE is the most notorious 100% of the volume) the 42-L ADs. The semi-industrial prion disease, which has cost the Canadian cattle industry AD was fed with fresh swine manure with a retention approximately $6.3 billion since 2003, as a result of closed time of 14 days. At the time of inoculation of the markets and consumer concerns over food safety issues 42-L ADs, the semi-industrial 7 m3 AD had been operat- related to it (http://www1.agric.gov.ab.ca). Therefore, the ing at 25 °C for more than 2 years. control and inactivation of prions from cattle carcasses Feather bags were added to two 42-L ADs (feather ADs during processing have been major public and animal with duplicate) at different times. Fourteen bags (No.1 to health concerns (Hill et al., 1997). No.14) were added to each AD on day 0 [initial load À1 In this study, ground feathers were added in bags to 0.88g g VSS (volatile suspended solid) manure, repre- ADs inoculated with adapted swine manure for methane senting 30% of the total Chemical oxygen demand production. The keratin-hydrolyzing organisms (KHOs) (COD) in each AD]. Three bags (from bags No.15 to responsible for the feather digestion were detected micro- No. 26) were added at day 22, day 55, day 85, and day scopically by BODIPY fluorescent protease staining 113. The other two ADs (control ADs with duplicate) (BODIPY FL casein staining) and further identified using were operated without addition of feather bags serving as the full-cycle rRNA approach (Amann et al., 1995). A 16S negative controls. The volume of the inoculum for these rRNA clone library was constructed from the bacterial four ADs was 35 L. All ADs were operated in a closed populations attached to feather particles inside feather room at 25 °C for 153 days. bags. Oligonucleotide FISH probes were designed to tar- get the major clusters of the 16S rRNA gene clones Physiochemical characterization of anaerobic retrieved and used to identify the KHOs in situ. digesters Total solids, volatile solids, total suspended solids (TSS), Materials and methods and volatile suspended solids were determined according to standard methods (APHA, 1998). Soluble COD was Source and preparation of chicken feathers determined according to the closed reflux colorimetric Freshly plucked white chicken feathers were collected method described in the standard methods. Methane from a slaughterhouse (Saint-Anselme, QC, Canada) and (CH4), total Kjeldahl nitrogen
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