The Mechanism of Sodium Sulfate Coupled with Anaerobic Methane Oxidation Mitigating Methane Production in Beef Cattle
Abstract
:1. Introduction
2. Materials and Methods
2.1. Experimental Design
2.2. Management of Experimental Animal
2.3. Experiment Method
2.4. Measurement Indicators and Methods
2.5. Statistical Analysis
3. Results
3.1. Effect of Different Sulfur Concentrations on Gas Production and Fermentation Parameters In Vitro
3.2. Effect of Different Sulfur Concentrations on the Gas Composition of Rumen Fermentation In Vitro
3.3. Effect of Different Sulfur Concentrations on Rumen Fermentation Parameters In Vitro
3.4. PCR Validation of Methane Anaerobic Oxidizing Archaea and Optimization of PCR
3.5. Effect of Different Sulfur Concentrations on Archaea, Bacteria, SRB and ANME
4. Discussion
4.1. Effect of Adding Na2SO4 on Gas Production Parameters and Gas Composition
4.2. Effect of Adding Na2SO4 on Fermentation Parameters In Vitro
4.3. Effect of Adding Na2SO4 on S-DAMO in the Rumen
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Amanullah, S.M.; Kim, D.H.; Paradhipta, D.H.; Lee, H.J.; Joo, Y.H.; Lee, S.S.; Kim, E.T.; Kim, S.C. Effects of Essential Fatty Acid Supplementation on in vitro Fermentation Indices, Greenhouse Gas, Microbes, and Fatty Acid Profiles in the Rumen. Front. Microbiol. 2021, 12, 637220. [Google Scholar] [CrossRef]
- Carolyn, O.; Gerber, P.; Anne, M.; Alessandra, F.; Giuseppe, T.; Michael, M.; Theun, V.; Henderson, B.; Steinfeld, H. Greenhouse Gas Emissions from Ruminant Supply Chains—A Global Life Cycle Assessment. 2013. Available online: https://www.sidalc.net/search/Record/dig-fao-it-20.500.14283-I3461E/Description (accessed on 29 August 2024).
- Sandeep, U.; Chaudhary, L.C.; Anju, K.; Neeta, A.; Chaturvedi, V.B. Effect of supplementing sulphate-reducing bacteria along with sulphur on growth performance, nutrient utilization and methane emission in goats. Trop. Anim. Health Prod. 2022, 55, 3. [Google Scholar] [CrossRef]
- Hao, W.; Qingxiang, M.; Zhongtang, Y. Effect of pH buffering capacity and sources of dietary sulfur on rumen fermentation, sulfide production, methane production, sulfate reducing bacteria, and total Archaea in in vitro rumen cultures. Bioresour. Technol. 2015, 186, 25–33. [Google Scholar] [CrossRef]
- Wu, H.; Li, Y.; Meng, Q.; Zhou, Z. Effect of High Sulfur Diet on Rumen Fermentation, Microflora, and Epithelial Barrier Function in Steers. Animals 2021, 11, 2545. [Google Scholar] [CrossRef] [PubMed]
- Zhao, Y.; Xie, B.; Gao, J.; Zhao, G. Dietary Supplementation with Sodium Sulfate Improves Rumen Fermentation, Fiber Digestibility, and the Plasma Metabolome through Modulation of Rumen Bacterial Communities in Steers. Appl. Environ. Microbiol. 2020, 86, e01412-20. [Google Scholar] [CrossRef]
- Yuxing, Z.; Jian, G.; Baohua, X.; Guanglei, Z. Comparison between the effects of feeding copper sulphate-treated and untreated rapeseed cake containing high glucosinolates on rumen fermentation, nutrient digestion and nitrogen metabolism in steers. J. Anim. Physiol. Anim. Nutr. 2021, 105, 849–860. [Google Scholar] [CrossRef]
- Wang, C.; Liqiang, H.; Zhang, G.W.; Hai, D.; Zhimei, W.; Liu, Q.; Gang, G.; Weiguang, H.; Zhang, J.; Zhang, Y.L.; et al. Effects of copper sulphate and coated copper sulphate addition on lactation performance, nutrient digestibility, ruminal fermentation and blood metabolites in dairy cows. Br. J. Nutr. 2020, 125, 251–259. [Google Scholar] [CrossRef]
- Zhao, Y.; Zhao, G. Decreasing ruminal methane production through enhancing the sulfate reduction pathway. Anim. Nutr. 2022, 9, 320–326. [Google Scholar] [CrossRef] [PubMed]
- Sara, L.C.; James, R.L.; Elizabeth, B.; Jed, O.E.; Sean, C.S.; Frederick, S.C. Anaerobic Oxidation of Methane: Mechanisms, Bioenergetics, and the Ecology of Associated Microorganisms. Environ. Sci. Technol. 2008, 44, 3200. [Google Scholar] [CrossRef]
- Xu, X.X.; Wang, J.K. Researeh progress on coupling of methanogenesis and anaerobic methane oxidation in the rumen. J. Ofzhejiang Univ. 2020, 46, 519–528. [Google Scholar] [CrossRef]
- Shen, L.; Hu, B.; Zheng, P. Progress in study on microorganisms responsiblefor anaerobic oxidation of methane. ACTA Pedol. Sin. 2011, 46, 519–528. [Google Scholar]
- Yongliang, M.; Xing-e, Q.; Aorui, L.; Xinfang, Z.; Zhongjun, J. Active Methanotrophs in Suboxic Alpine Swamp Soils of the Qinghai–Tibetan Plateau. Front. Microbiol. 2020, 11, 580866. [Google Scholar] [CrossRef]
- Marc, J.A.; Tori, M.H. Anaerobic methane oxidation by archaea/sulfate-reducing bacteria aggregates: 1. Thermodynamic and physical constraints. Am. J. Sci. 2009, 309, 869–957. [Google Scholar] [CrossRef]
- Menke, K.H. Estimation of the energetic feed value obtained from chemical analysis and in vitro gas production using rumen fluid. Anim. Res. Dev. 1988, 28, 7–55. [Google Scholar]
- Ken, T.; Koki, H. Rapid Detection and Quantification of Members of the Archaeal Community by Quantitative PCR Using Fluorogenic Probes. Appl. Environ. Microbiol. 2000, 66, 5066–5072. [Google Scholar]
- DELONG, E.F. Archaea in coastal marine environments. Proc. Natl. Acad. Sci. USA 1992, 89, 5685–5689. [Google Scholar] [CrossRef]
- Rudolf, A.; Brian, J.B.; Robert, J.O.; Sallie, W.C.; Richard, D.; David, A.S. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 1990, 56, 1919–1925. [Google Scholar] [CrossRef]
- Peer, H.A.T.; Jarno, G.; Widjaja-Greefkes, H.C.A.; Caroline, M.P.; Alfons Johannes Maria, S.; Piet, N.L.L.; Roel, J.W.M. Growth of Anaerobic Methane-Oxidizing Archaea and Sulfate-Reducing Bacteria in a High-Pressure Membrane Capsule Bioreactor. Appl. Environ. Microbiol. 2015, 81, 1286–1296. [Google Scholar] [CrossRef]
- Peter, R.G.; Victoria, J.O.; Steven, J.H.; Edward, F.D. Growth and Methane Oxidation Rates of Anaerobic Methanotrophic Archaea in a Continuous-Flow Bioreactor. Appl. Environ. Microbiol. 2003, 69, 5472–5482. [Google Scholar] [CrossRef]
- Alemu, F. Identification and quantitation of mucosal and faecal desulfovibrios using real time polymerase chain reaction. Gut 2004, 53, 523–529. [Google Scholar] [CrossRef]
- Patra, A.K.; Yu, Z. Combinations of nitrate, saponin, and sulfate additively reduce methane production by rumen cultures in vitro while not adversely affecting feed digestion, fermentation or microbial communities. Bioresour Technol. 2014, 155, 129–135. [Google Scholar] [CrossRef] [PubMed]
- Martin, H.; McGinn, S.M.; Beauchemin, K.A.; Okine, E.K.; Odd Magne, H.; Tim, A.M. Effect of dried distillers grains plus solubles on enteric methane emissions and nitrogen excretion from growing beef cattle1. J. Anim. Sci. 2013, 91, 2846–2857. [Google Scholar] [CrossRef]
- Pattaya, N.; Chalong, W.; Saenjan, P.; Yuangklang, C. Effect of Sulfate-Containing Compounds on Methane Production by Using an In vitro Gas Production Technique. Pak. J. Nutr. 2013, 12, 723–729. [Google Scholar] [CrossRef]
- Abdl-Rahman, M.A.; Sawiress, F.A.R.; El-Aty, A.M.A. Effect of Sodium Lauryl Sulfate-Fumaric Acid Coupled Addition on theIn VitroRumen Fermentation with Special Regard to Methanogenesis. Vet. Med. Int. 2010, 2010, 858474. [Google Scholar] [CrossRef]
- Marlow, J.J.; Skennerton, C.T.; Li, Z.; Chourey, K.; Hettich, R.L.; Pan, C.; Orphan, V.J. Proteomic Stable Isotope Probing Reveals Biosynthesis Dynamics of Slow Growing Methane Based Microbial Communities. Front. Microbiol. 2016, 7, 563. [Google Scholar] [CrossRef]
- Silvan, S.; Meike, G.; Reinhard, B.; Rudolf, K.T.; Bernhard, J. The key nickel enzyme of methanogenesis catalyses the anaerobic oxidation of methane. Nature 2010, 465, 606–608. [Google Scholar] [CrossRef]
- Ma, Y.; Liu, N.; Greisen, P.; Li, J.; Qiao, K.; Huang, S.; Stephanopoulos, G. Removal of lycopene substrate inhibition enables high carotenoid productivity in Yarrowia lipolytica. Nat. Commun. 2022, 13, 572. [Google Scholar] [CrossRef] [PubMed]
- Wei, L.; Xiaokun, H.; Cong-Qiang, L.; Hu, D.; Mingxuan, L.; Fangyuan, S.; Siliang, L.; Yunchao, L. Sulfate concentrations affect sulfate reduction pathways and methane consumption in coastal wetlands. Water Res. 2022, 217, 118441. [Google Scholar] [CrossRef]
- Liu, J.X.; Chen, H.; Xue, D.; Gao, Y.H.; Liu, J.L.; Yang, J. Advances in microbial mediated anaerobic oxidation of methane and its influencing factors. Chin. Joumal Ecol. 2020, 39, 1033–1044. [Google Scholar] [CrossRef]
- Emma, B.; Tiina, L.; Johannes, A.; Anders, F.A.; Qian, C.; Weili, X.; Robert, L.H.; Louise, B.; Manon, F.; Guillaume, S.; et al. Biogeochemical Cycling by a Low-Diversity Microbial Community in Deep Groundwater. Front. Microbiol. 2018, 9, 2129. [Google Scholar] [CrossRef]
- Damian Jesus Nahuel, C.; María Esperanza, C.-C.; Abimael, O.-C.; Gustavo, D.; José Matías, I.; Ariel, A.; Silvio, C.; Germán, C. Ruminal effects of excessive dietary sulphur in feedlot cattle. J. Anim. Physiol. Anim. Nutr. 2021, 106, 978–987. [Google Scholar] [CrossRef]
- Gould, D.H.; Cummings, B.A.; Hamar, D.W. In vivo indicators of pathologic ruminal sulfide production in steers with diet-induced polioencephalomalacia. J. Vet. Diagn. Investig. 1997, 9, 72–76. [Google Scholar] [CrossRef] [PubMed]
- Slyter, L.L.; William, C.; Oltjen, R.R.; Weaver, J.M. Sulfur Influences on Rumen Microorganisms In Vitro and in Sheep and Calves. J. Anim. Sci. 1986, 63, 1949–1959. [Google Scholar] [CrossRef]
- Thao, N.T.; Wanapat, M.; Cherdthong, A.; Kang, S. Effects of eucalyptus crude oils supplementation on rumen fermentation, microorganism and nutrient digestibility in swamp buffaloes. Asian-Australas J. Anim. Sci. 2014, 27, 46–54. [Google Scholar] [CrossRef]
- Haroon, M.F.; Hu, S.; Shi, Y.; Imelfort, M.; Keller, J.; Hugenholtz, P.; Yuan, Z.; Tyson, G.W. Erratum: Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature 2013, 501, 578. [Google Scholar] [CrossRef]
- Katrin, K.; Antje, B. Anaerobic Oxidation of Methane: Progress with an Unknown Process. Annu. Rev. Microbiol. 2009, 63, 311–334. [Google Scholar] [CrossRef]
- Antje, B.; Katrin, R.; Carsten, J.S.; Dirk, R.; Friedrich, W.; Armin, G.; Rudolf, A.; Bo Barker, J.; Ursula, W.; Olaf, P. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 2000, 407, 623–626. [Google Scholar] [CrossRef]
- Katrin, K.; Tina, L.; Antje, B.; Renate, K.; Rudolf, A. Diversity and Distribution of Methanotrophic Archaea at Cold Seeps. Appl. Environ. Microbiol. 2005, 71, 467–479. [Google Scholar] [CrossRef]
- Walter, M.; Richard, S.; Katja, N.; Tina, T.; Volker, T.; Martin, B.; Katrin, K.; Armin, G.; Peterknecht, K.; Thomas, P.; et al. Microbial Reefs in the Black Sea Fueled by Anaerobic Oxidation of Methane. Science 2002, 297, 1013–1015. [Google Scholar] [CrossRef]
Items | Contents |
---|---|
Ingredients (g/kg DM) | |
Whole plant corn silage | 310.00 |
Corn stalker | 130.00 |
Ground corn | 320.00 |
Jujube powder | 60.00 |
Soybean meal | 80.00 |
Palm meal | 60.00 |
Premix | 17.00 |
Sodium bicarbonate | 8.00 |
Salt | 10.00 |
Total | 1000.00 |
Nutritional composition | |
ME (MJ/kg) | 10.72 |
CP (%DM) | 9.88 |
NDF (%DM) | 49.02 |
ADF (%DM) | 22.92 |
Ca (%DM) | 0.60 |
P (%DM) | 0.27 |
S (%DM) | 0.40 |
Na2SO4 (%DM) | 0.00 |
Items | Reaction System 50 μL |
---|---|
2 × Ultra SYBR Mixture (High ROX) | 25 |
Primer-Forward (μM) | 1 |
Primer-Reverse (μM) | 1 |
Template DNA | 2 |
ddH2O | up to 50 |
Items | Treatments | SEM | p-Value | p-Value | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
0.4% | 0.6% | 0.8% | 1.0% | 1.2% | 1.4% | 1.6% | 1.8% | 2.0% | 2.2% | 2.4% | L | Q | |||
Gas production (mL/0.2 g DM) | |||||||||||||||
24 h | 54.07 | 49.57 | 52.47 | 52.57 | 51.03 | 49.30 | 49.13 | 47.47 | 48.88 | 44.82 | 48.03 | 0.79 | 0.20 | <0.01 | 0.91 |
48 h | 58.60 | 53.60 | 56.53 | 56.47 | 54.83 | 52.63 | 52.93 | 50.93 | 51.97 | 48.92 | 52.20 | 0.84 | 0.21 | <0.01 | 0.82 |
Gas production parameters | |||||||||||||||
B (mL/0.2 g DM) 1 | 58.10 | 52.94 | 55.97 | 55.98 | 54.47 | 52.26 | 52.12 | 50.70 | 51.69 | 48.41 | 52.16 | 0.72 | 0.24 | <0.01 | 0.57 |
C (h−1) 2 | 0.11 | 0.11 | 0.11 | 0.11 | 0.11 | 0.12 | 0.12 | 0.11 | 0.12 | 0.13 | 0.11 | <0.01 | 0.11 | 0.48 | 0.02 |
Items | Treatments | SEM | p-Value | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
0.4% | 0.6% | 0.8% | 1.0% | 1.2% | 1.4% | 1.6% | 1.8% | 2.0% | 2.2% | 2.4% | |||
CH4 (%) | 22.03 bcd | 20.38 a | 21.92 bcd | 20.51 a | 20.38 a | 21.16 abc | 20.81 ab | 21.13 abc | 21.08 abc | 22.68 d | 22.17 cd | 0.24 | <0.01 |
H2S (ppm) | 1237.83 a | 2314.14 b | 2326.56 b | 2678.64 c | 2646.91 c | 2549.34 c | 2534.57 c | 2701.84 c | 3127.49 d | 3062.67 d | 3064.56 d | 157.66 | <0.01 |
Items | Sulfur Concentration (%) | CH4 (%) | CO2 (%) |
---|---|---|---|
Sulfur concentration (%) | 1 | ||
CH4 (%) | −0.628 ** | 1 | |
CO2 (%) | 0.346 | −0.478 ** | 1 |
Items | Treatments | SEM | p-Value | p-Value | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
0.4% | 0.6% | 0.8% | 1.0% | 1.2% | 1.4% | 1.6% | 1.8% | 2.0% | 2.2% | 2.4% | L | Q | |||
24 h Fermentation parameter | |||||||||||||||
pH | 6.61 | 6.61 | 6.60 | 6.56 | 6.58 | 6.58 | 6.59 | 6.57 | 6.61 | 6.64 | 6.58 | <0.01 | 0.63 | 0.19 | 0.66 |
NH3-N 1 (mg/100 mL) | 13.09 | 14.94 | 12.17 | 14.80 | 11.99 | 13.09 | 12.72 | 11.99 | 14.80 | 12.80 | 15.12 | 0.38 | 0.46 | 0.40 | 0.08 |
TVFA 2 (mmol/L) | 71.99 | 72.55 | 61.84 | 66.72 | 66.60 | 70.20 | 65.81 | 67.64 | 80.09 | 58.34 | 58.94 | 1.92 | 0.80 | 0.45 | 0.71 |
Acetate (%) | 65.56 | 63.99 | 63.96 | 64.40 | 64.63 | 64.78 | 65.93 | 64.91 | 66.85 | 64.68 | 63.60 | 0.29 | 0.73 | 0.73 | 0.57 |
Propionate (%) | 17.52 | 17.36 | 17.28 | 17.04 | 17.69 | 17.46 | 17.12 | 17.47 | 17.69 | 16.89 | 17.52 | 0.08 | 0.06 | 0.68 | 0.59 |
Isobutyrate (%) | 1.64 | 1.76 | 1.76 | 1.78 | 1.67 | 1.70 | 1.65 | 1.65 | 1.55 | 1.74 | 1.82 | 0.02 | 0.82 | 0.86 | 0.52 |
Butyrate (%) | 11.13 | 11.96 | 12.06 | 11.59 | 11.59 | 11.70 | 10.91 | 11.47 | 10.47 | 11.68 | 11.99 | 0.15 | 0.66 | 0.64 | 0.64 |
Isovalerate (%) | 2.91 | 3.49 | 3.50 | 3.66 | 3.12 | 3.09 | 3.08 | 3.20 | 2.70 | 3.54 | 3.57 | 0.09 | 0.45 | 0.93 | 0.60 |
Valerate (%) | 1.23 | 1.45 | 1.43 | 1.52 | 1.29 | 1.27 | 1.31 | 1.29 | 1.04 | 1.46 | 1.50 | 0.04 | 0.46 | 0.82 | 0.53 |
A/P3 | 3.74 | 3.69 | 3.70 | 3.78 | 3.65 | 3.71 | 3.86 | 3.72 | 3.84 | 3.83 | 3.63 | 0.02 | 0.69 | 0.66 | 0.53 |
48 h Fermentation parameter | |||||||||||||||
pH | 6.67 | 6.66 | 6.62 | 6.60 | 6.61 | 6.61 | 6.61 | 6.65 | 6.66 | 6.64 | 6.64 | <0.01 | 0.33 | 0.96 | 0.02 |
NH3-N 1 (mg/100 mL) | 14.59 | 15.33 | 14.12 | 14.39 | 14.39 | 14.26 | 14.97 | 14.56 | 14.56 | 15.72 | 15.68 | 0.17 | 0.31 | 0.09 | 0.03 |
TVFA 2 (mmol/L) | 78.67 | 59.34 | 67.13 | 62.49 | 59.01 | 67.81 | 57.83 | 71.45 | 91.58 | 55.20 | 60.98 | 3.25 | 0.90 | 0.82 | 0.96 |
Acetate (%) | 60.44 | 64.00 | 65.05 | 65.47 | 61.98 | 66.64 | 63.99 | 65.92 | 72.50 | 65.43 | 68.31 | 0.96 | 0.24 | 0.04 | 0.89 |
Propionate (%) | 17.42 | 17.22 | 17.02 | 16.64 | 17.22 | 16.58 | 17.16 | 16.73 | 14.21 | 17.30 | 16.19 | 0.27 | 0.55 | 0.14 | 0.93 |
Isobutyrate (%) | 2.43 | 2.02 | 1.91 | 1.94 | 2.29 | 1.79 | 2.10 | 1.90 | 1.48 | 1.92 | 1.70 | 0.08 | 0.41 | 0.04 | 0.86 |
Butyrate (%) | 13.10 | 11.37 | 11.09 | 10.82 | 12.42 | 10.41 | 11.49 | 10.59 | 8.00 | 10.67 | 9.51 | 0.41 | 0.40 | 0.03 | 0.94 |
Isovalerate (%) | 4.73 | 3.89 | 3.62 | 3.69 | 4.34 | 3.31 | 3.81 | 3.51 | 2.80 | 3.41 | 3.11 | 0.16 | 0.50 | 0.03 | 0.77 |
Valerate (%) | 1.89 | 1.49 | 1.37 | 1.43 | 1.75 | 1.28 | 1.45 | 1.35 | 1.01 | 1.27 | 1.17 | 0.07 | 0.31 | 0.02 | 0.80 |
A/P 3 | 3.47 | 3.72 | 3.94 | 3.95 | 3.60 | 4.02 | 3.73 | 3.94 | 6.01 | 3.78 | 4.25 | 0.21 | 0.52 | 0.14 | 0.96 |
Name | Primer | Citation | Annealing Temperature |
---|---|---|---|
Archaea 806F/958R | 5’-ATT AGA TAC CCS BGT AGT CC-3’ 5’-YCC GGC GTT GAM TCC AAT T-3’ | [16,17] | 55.0 °C |
Bacteria BAC27F/EUB338R | 5’-AGA GTT TGA TCC TGG CTC AG-3’ 5’-GCT GCC TCC CGT AGG AGT-3’ | [17,18] | 55.0 °C |
ANME-1 1337F/1724R | 5’-AGG TCC TAC GGG ACG CAT-3’ 5’-GGT CAG ACG CCT TCG CT-3’ | [19] | 54.4 °C |
ANME-2c 468F/736R | 5’-CGC ACA AGA TAG CAA GGG-3’ 5’-CGT CAG ACC CGT TCT GGT A-3’ | [20] | 56.3 °C |
SRB 691F/826R | 5’-CCG TAG ATA TCT GGA GGA ACA TCA G-3’ 5’-ACA TCT AGC ATC CAT CGT TTA CAG C-3’ | [21] | 60.0 °C |
Items | Treatments | SEM | p-Value | p-Value | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
0.4% | 0.6% | 0.8% | 1.0% | 1.2% | 1.4% | 1.6% | 1.8% | 2.0% | 2.2% | 2.4% | L | Q | |||
Archaea (log10 no.of copies) | 5.09 a | 5.62 c | 5.52 ab | 5.13 a | 5.14 a | 5.11 a | 5.42 b | 5.15 ab | 5.08 a | 5.48 ab | 5.84 d | 0.08 | <0.01 | <0.01 | <0.01 |
Bacteria (log10 no.of copies) | 6.95 | 6.65 | 6.80 | 6.14 | 6. 59 | 6.83 | 6.84 | 6.90 | 6.56 | 6.56 | 6.59 | 0.08 | 0.98 | 0.48 | 0.63 |
ANME-1 1 (log10 no.of copies) | 2.77 cd | 2.82 de | 2.19 a | 2.70 c | 2.44 b | 2.49 b | 3.10 h | 2.73 c | 2.69 c | 2.96 fg | 2.88 ef | 0.08 | <0.01 | <0.01 | <0.01 |
ANME-2c 2 (log10 no.of copies) | 3.41 a | 3.72 cd | 3.50 ab | 3.63 bcd | 3.61 bcd | 3.59 bc | 4.06 f | 3.78 de | 3.69 cd | 3.96 f | 3.91 ef | 0.06 | <0.01 | <0.01 | 0.33 |
SRB 3 (log10 no.of copies) | 1.56 a | 1.60 ab | 1.48 a | 1.46 a | 1.53 a | 1.45 a | 1.72 bc | 1.54 a | 1.52 a | 1.77 c | 1.98 d | 0.05 | <0.01 | <0.01 | <0.01 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Zhu, X.; Zhou, Z.; Cheng, Y.; Deng, Z.; Wu, H.; Nussio, L.G.; Zhou, Z.; Meng, Q. The Mechanism of Sodium Sulfate Coupled with Anaerobic Methane Oxidation Mitigating Methane Production in Beef Cattle. Microorganisms 2024, 12, 1825. https://doi.org/10.3390/microorganisms12091825
Zhu X, Zhou Z, Cheng Y, Deng Z, Wu H, Nussio LG, Zhou Z, Meng Q. The Mechanism of Sodium Sulfate Coupled with Anaerobic Methane Oxidation Mitigating Methane Production in Beef Cattle. Microorganisms. 2024; 12(9):1825. https://doi.org/10.3390/microorganisms12091825
Chicago/Turabian StyleZhu, Xiaowen, Zhiyu Zhou, Yang Cheng, Ziqi Deng, Hao Wu, Luiz Gustavo Nussio, Zhenming Zhou, and Qingxiang Meng. 2024. "The Mechanism of Sodium Sulfate Coupled with Anaerobic Methane Oxidation Mitigating Methane Production in Beef Cattle" Microorganisms 12, no. 9: 1825. https://doi.org/10.3390/microorganisms12091825