T4-like Phages Reveal the Potential Role of Viruses in Soil Organic Matter Mineralization

Viruses are the most abundant biological entities in the world, but their ecological functions in soil are virtually unknown. We hypothesized that greater abundance of T4-like phages will increase bacterial death and thereby suppress soil organic carbon (SOC) mineralization. A range of phage and bacterial abundances were established in sterilized soil by reinoculation with 10-3 and 10-6 dilutions of suspensions of unsterilized soil. The total and viable 16S rRNA gene abundance (a universal marker for bacteria) was measured by qPCR to determine bacterial abundance, with propidium monoazide (PMA) preapplication to eliminate DNA from non-viable cells. Abundance of the g23 marker gene was used to quantify T4-like phages. A close negative correlation between g23 abundance and viable 16S rRNA gene abundance was observed. High abundance of g23 led to lower viable ratios for bacteria, which suggested that phages drove microbial necromass production. The CO2 efflux from soil increased with bacterial abundance but decreased with higher abundance of T4-like phages. Elimination of extracellular DNA by PMA strengthened the relationship between CO2 efflux and bacterial abundance, suggesting that SOC mineralization by bacteria is strongly reduced by the T4-like phages. A random forest model revealed that abundance of T4-like phages and the abundance ratio of T4-like phages to bacteria are better predictors of SOC mineralization (measured as CO2 efflux) than bacterial abundance. Our study provides experimental evidence of phages' role in organic matter turnover in soil: they can retard SOC decomposition but accelerate bacterial turnover. © 2021 American Chemical Society. All rights reserved.

Wei X.1 , Ge T.1, 2 , Wu C.2 , Wang S.2 , Mason-Jones K.3 , Li Y. 4 , Zhu Z.1 , Hu Y.1 , Liang C.5 , Shen J.1 , Wu J.1 , Kuzyakov Y. 6, 7
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  • 1 Key Lab. of Agro-Ecol. Processes in Subtropic. Reg. and Changsha Res. Stn. for Agric. and Environ. Monitoring, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, 410125, China
  • 2 State Key Lab. for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Key Laboratory of Biotechnology in Plant Protection, Ministry of Agriculture and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China
  • 3 Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, 106708, Netherlands
  • 4 Zhejiang Provincial Key Laboratory of Agricultural Resources and Environment, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou, 310058, China
  • 5 Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, 110016, China
  • 6 Department of Soil Science of Temperate Ecosystems, University of Goettingen, Goettingen, 37073, Germany
  • 7 Agro-Technological Institute, RUDN University, Moscow, 117198, Russian Federation
Bacteria; Biogeochemistry; Carbon dioxide; Decision trees; Genes; Mineralogy; Organic carbon; Polymerase chain reaction; RNA; Soils; Biological entities; Ecological functions; Experimental evidence; Negative correlation; Organic matter turnovers; Random forest modeling; Soil organic carbon; Soil organic matter mineralizations; Bacteriophages; carbon dioxide; endogenous compound; organic carbon; organic matter; RNA 16S; soil organic matter; carbon; cell component; mineralization; soil organic matter; virus; Article; bacterial gene; bacterial growth; bacteriophage; carbon mineralization; controlled study; decomposition; DNA extraction; gene dosage; marker gene; microbial community; mineralization; nonhuman; population abundance; population size; random forest; real time polymerase chain reaction; soil analysis; soil microflora; treatment response; virus; genetics; microbiology; soil; Bacteria (microorganisms); T4-like viruses; Bacteriophages; Carbon; RNA, Ribosomal, 16S; Soil; Soil Microbiology
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