pH selects for distinct N2O-reducing microbiomes in tropical soil microcosms

Author:

Sun Yanchen123,Yin Yongchao245,He Guang6,Cha Gyuhyon7,Ayala-del-Río Héctor L8,González Grizelle9,Konstantinidis Konstantinos T7,Löffler Frank E1246

Affiliation:

1. Department of Civil and Environmental Engineering, University of Tennessee , Knoxville, Knoxville, TN 37996 , United States

2. Center for Environmental Biotechnology, University of Tennessee , Knoxville, Knoxville, TN 37996 , United States

3. Present address: Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution , Woods Hole, MA 02543 , United States

4. Department of Microbiology, University of Tennessee , Knoxville, Knoxville, TN 37996 , United States

5. Present address: Department of Biology, Antimicrobial Discovery Center, Northeastern University , Boston, MA 02148 , United States

6. Department of Biosystems Engineering and Soil Science, University of Tennessee , Knoxville, Knoxville, TN 37996 , United States

7. School of Civil and Environmental Engineering, Georgia Institute of Technology , Atlanta, GA 30332 , United States

8. Department of Biology, University of Puerto Rico at Humacao , Humacao 00792 , Puerto Rico

9. USDA Forest Service, International Institute of Tropical Forestry , San Juan 00926 , Puerto Rico

Abstract

Abstract Nitrous oxide (N2O), a greenhouse gas with ozone destruction potential, is mitigated by the microbial reduction to dinitrogen catalyzed by N2O reductase (NosZ). Bacteria with NosZ activity have been studied at circumneutral pH but the microbiology of low pH N2O reduction has remained elusive. Acidic (pH < 5) tropical forest soils were collected in the Luquillo Experimental Forest in Puerto Rico, and microcosms maintained with low (0.02 mM) and high (2 mM) N2O assessed N2O reduction at pH 4.5 and 7.3. All microcosms consumed N2O, with lag times of up to 7 months observed in microcosms with 2 mM N2O. Comparative metagenome analysis revealed that Rhodocyclaceae dominated in circumneutral microcosms under both N2O feeding regimes. At pH 4.5, Peptococcaceae dominated in high-N2O, and Hyphomicrobiaceae in low-N2O microcosms. Seventeen high-quality metagenome-assembled genomes (MAGs) recovered from the N2O-reducing microcosms harbored nos operons, with all eight MAGs derived from acidic microcosms carrying the Clade II type nosZ and lacking nitrite reductase genes (nirS/K). Five of the eight MAGs recovered from pH 4.5 microcosms represent novel taxa indicating an unexplored N2O-reducing diversity exists in acidic tropical soils. A survey of pH 3.5–5.7 soil metagenome datasets revealed that nosZ genes commonly occur, suggesting broad distribution of N2O reduction potential in acidic soils.

Funder

US National Science Foundation

China Scholarship Council

Publisher

Oxford University Press (OUP)

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