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Current Advances in Molecular Methods for Detection of Nitrite-Dependent Anaerobic Methane Oxidizing Bacteria in Natural Environments

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Current Advances in Molecular Methods for Detection of Nitrite-Dependent Anaerobic Methane Oxidizing Bacteria in Natural Environments Original citation: Chen, Jing, Dick, Richard, Lin, Jih-Gaw and Gu, Ji-Dong. (2016) Current advances in molecular methods for detection of nitrite-dependent anaerobic methane oxidizing bacteria in natural environments. Applied Microbiology and Biotechnology, 100 (23). pp. 9845-9860. Permanent WRAP URL: http://wrap.warwick.ac.uk/86286 Copyright and reuse: The Warwick Research Archive Portal (WRAP) makes this work by researchers of the University of Warwick available open access under the following conditions. Copyright © and all moral rights to the version of the paper presented here belong to the individual author(s) and/or other copyright owners. To the extent reasonable and practicable the material made available in WRAP has been checked for eligibility before being made available. 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For more information, please contact the WRAP Team at: [email protected] warwick.ac.uk/lib-publications 1 Current Advances in Molecular Methods for Detection of 2 Nitrite-dependent Anaerobic Methane Oxidizing Bacteria in Natural 3 Environments 4 5 Jing Chen1,2, Richard Dick3, Jih-Gaw Lin4, and Ji-Dong Gu1* 6 7 1 Laboratory of Environmental Microbiology and Toxicology, School of Biological 8 Sciences, Faculty of Science, The University of Hong Kong, Pokfulam Road, Hong Kong 9 SAR, P.R. China 10 2 Currently Address: School of Life Sciences, University of Warwick, Coventry, United 11 Kingdom 12 3 School of Environment and Natural Resources, College of Food, Agricultural, and 13 Environmental Sciences, The Ohio State University, Columbus, OH, USA 14 4 Institute of Environmental Engineering, National Chiao Tung University, Hsinchu, 15 Taiwan 30010 16 17 *Corresponding author 18 Mailing address: School of Biological Sciences, The University of Hong Kong, Pokfulam 19 Road, Hong Kong SAR, P.R. China 20 Tel: 852-2299-0605; Fax: 852-2559-9114; E-mail: [email protected] - 1 - 21 Abstract 22 Nitrite-dependent anaerobic methane oxidation (n-damo) process uniquely links microbial 23 nitrogen and carbon cycles. Research on n-damo bacteria progresses quickly with 24 experimental evidences through enrichment cultures. Polymerase chain reaction 25 (PCR)-based methods for detecting them in various natural ecosystems and engineered 26 systems play a very important role in the discovery of their distribution, abundance and 27 biodiversity in the ecosystems. Important characteristics of n-damo enrichments were 28 obtained and their key significance in microbial nitrogen and carbon cycles was 29 investigated. The molecular methods currently used in detecting n-damo bacteria were 30 comprehensively reviewed and discussed for their strengths and limitations in applications 31 with a wide range of samples. The pmoA gene-based PCR primers for n-damo bacterial 32 detection were evaluated and, in particular, several incorrectly stated PCR primer 33 nucleotide sequences in the published papers were also pointed out to allow correct 34 applications of the PCR primers in current and future investigations. Furthermore, this 35 review also offers the future perspectives of n-damo bacteria based on current information 36 and methods available for a better acquisition of new knowledge about this group of 37 bacteria. 38 39 Keywords: n-damo; anaerobic methane oxidation; denitrification; Methylomirabilis 40 oxyfera-like bacteria; molecular detection; PCR primer; pmoA gene - 2 - 41 Introduction 42 Biological denitrification process has been investigated for more than half a century (Hill 43 1979; Keeney et al. 1971; McGarity 1961). However, the anaerobic methane oxidation 44 coupled to denitrification was once considered only thermodynamically feasible before the 45 experimental evidences obtained in 2006 (Raghoebarsing et al. 2006). There was no direct 46 evidence of any microorganisms capable of coupling methane oxidation and denitrification 47 under anoxic conditions (Knowles 2005; Mason 1977; Strous and Jetten 2004), although the 48 process can provide enough energy as shown in the following equations (Raghoebarsing et al. 49 2006). 50 5 CH4 8 NO 3 8 H 5 CO 2 + 4 N 2 + 14 H 2 O [1] 1 51 (G 765 kJ mol CH4 ) 52 3 CH4 8 NO 2 8 H 3 CO 2 + 4 N 2 + 10 H 2 O [2] 1 53 (G 928 kJ mol CH4 ) 54 Obtained from the anoxic sediments, a microbial consortium consisting of two 55 microorganisms (a bacterium belonging to NC10 phylum without any cultured species and an 56 archaeon distantly clustering with marine methanotrophic Archaea) showed a denitrification -1 57 rate of 21.5 ± 2 μmol N2 h with the simultaneous conversion of the added methane at a rate -1 58 of 22.0 ± 2 μmol CH4 h (Raghoebarsing et al. 2006). Using the enrichment culture of 59 Raghoebarsing et al. (2006) as inocula, Ettwig et al. (2008) demonstrated that the specific 60 inhibitor, Bromoethane at a concentration of 20 mM, for the key mcr gene of methanotrophic 61 and methanogenic archaea showed no effect on the subculture oxidizing methane and 62 reducing nitrite, which was further enhanced with the decline of the archaeal population. - 3 - - 63 Results showed a stoichiometry of 8: 3.5 for NO2 : CH4 after 22 months of enrichment, very 64 close to the above equations (Ettwig et al. 2008). 65 A comparison of the parameters and results of several n-damo enrichments is presented in 66 Table 1. Some important characteristics of n-damo inocula in these studies (Ettwig et al. 2008; 67 Ettwig et al. 2009; Hu et al. 2009; Hu et al. 2011; Luesken et al. 2011a; Luesken et al. 2011b; 68 Zhu et al. 2011) are: first, no pure culture of n-damo bacteria is available and the enrichments 69 so far contained around 30-80% of NC10 phylum bacteria closely related to M. oxyfera (Shen 70 et al. 2015b); second, almost all of the n-damo enrichments were successfully established 71 from freshwater habitats as inocula, including wastewater treatment plant (WWTP). One 72 investigation reported that the highest n-damo activity was achieved without NaCl addition 73 into the culture medium in a study on the effect of a range of NaCl concentrations (0-20 g 74 NaCl L-1) (He et al. 2015b). Only very recently, a halophilic denitrifying methanotrophic 75 culture (optimal salinity of 20‰) was obtained after 20 months of enrichment based on the 76 microbial community in the coastal mudflat sediment, of which the active species belonged to 77 NC10 bacteria (He et al. 2015a). Third, n-damo enrichment usually requires a very long 78 culturing and enriching period before the activity can be detected and stable. Ettwig et al. 79 (2009) reported that there was no measurable n-damo activity before 110 days in the 80 enrichment, and then it started to be detectable and increase. The estimated doubling time for 81 n-damo bacteria is one to two weeks under laboratory condition (Ettwig et al. 2008) with a 82 methane conversion rate of 1.7 nmol min-1 mg protein-1 (Ettwig et al. 2009). Finally, n-damo 83 bacteria are often simultaneously co-cultured with anaerobic ammonium oxidizing (anammox) 84 bacteria (Luesken et al. 2011a; Zhu et al. 2011), which also used nitrite as electron acceptor, - 4 - 85 but utilized ammonium as electron donor instead of methane under anaerobic conditions. We 86 would like to make an updated evaluation of the current PCR primers available for detection 87 of n-damo and in particular point out the error in some of the published PCR primer set, 88 which has been widely used in molecular detection of n-damo. Such awareness is necessary 89 so that the science and new knowledge can be built systematically on sound foundation. 90 91 Significance of n-damo bacteria in microbial nitrogen and carbon cycles 92 Microbial process couples anaerobic methane oxidation to denitrification 93 Microbes capable of simultaneously oxidizing methane and denitrifying anaerobically had 94 not been found in nature nor isolated in pure culture (Knowles 2005; Strous and Jetten 2004) 95 before the first report of direct evidence of anaerobic methane oxidation with denitrification 96 (Raghoebarsing et al. 2006). Ettwig et al. (2008) further showed that the microbial 97 consortium in the study of Raghoebarsing et al. (2006) could perform the n-damo process 98 without the presence of archaea. The active bacterium was named as Candidatus 99 Methylomirabilis oxyfera that could reduce nitrite to dinitrogen (N2) and utilize methane as 100 an electron donor under anaerobic conditions based on genomic analyses and experimental 101 results (Ettwig et al. 2010; Ettwig et al. 2008; Ettwig et al. 2009). This nitrite-driven 102 anaerobic oxidation of methane (AOM) provides a very unique link between the microbial 103 nitrogen and carbon cycles, previously unknown to science. Later on, Haroon et al. (2013) 104 reported a novel archaeal lineage, Candidatus Methanoperedens nitroreducens, which can 105 carry out AOM with reduction of nitrate to nitrite and needs the participation of anammox 106 bacteria to complete the denitrification process. Very recently, aerobic methanotroph - 5 - 107 Methylomonas denitrificans sp. nov. strain FJG1T was suggested to couple nitrate reduction 108 to methane oxidation under oxygen limitation, but oxygen was still required because M.
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