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Active Soil Nitrifying Communities Revealed by In Situ Transcriptomics and Microcosm-Based Stable-Isotope Probing.

ABSTRACT: Long-term nitrogen field fertilization often results in significant changes in nitrifying communities that catalyze a key step in the global N cycle. However, whether microcosm studies are able to inform the dynamic changes in communities of ammonia-oxidizing bacteria (AOB) and archaea (AOA) under field conditions remains poorly understood. This study aimed to evaluate the transcriptional activities of nitrifying communities under in situ conditions, and we found that they were largely similar to those of ¹³C-labeled nitrifying communities in the urea-amended microcosms of soils that had received different N fertilization regimens for 22 years. High-throughput sequencing of 16S rRNA genes and transcripts suggested that Nitrosospira cluster 3-like AOB and Nitrososphaera viennensis-like AOA were significantly stimulated in N-fertilized fresh soils. Real-time quantitative PCR demonstrated that the significant increase of AOA and AOB in fresh soils upon nitrogen fertilization could be preserved in the air-dried soils. DNA-based stable-isotope probing (SIP) further revealed the greatest labeling of Nitrosospira cluster 3-like AOB and Nitrosospira viennensis-like AOA, despite the strong advantage of AOB over AOA in the N-fertilized soils. Nitrobacter-like nitrite-oxidizing bacteria (NOB) played more important roles than Nitrospira-like NOB in urea-amended SIP microcosms, while the situation was the opposite under field conditions. Our results suggest that long-term fertilization selected for physiologically versatile AOB and AOA that could have been adapted to a wide range of substrate ammonium concentrations. It also provides compelling evidence that the dominant communities of transcriptionally active nitrifiers under field conditions were largely similar to those revealed in ¹³C-labeled microcosms.IMPORTANCE The role of manipulated microcosms in microbial ecology has been much debated, because they cannot entirely represent the in situ situation. We collected soil samples from 20 field plots, including 5 different treatments with and without nitrogen fertilizers for 22 years, in order to assess active nitrifying communities by in situ transcriptomics and microcosm-based stable-isotope probing. The results showed that chronic N enrichment led to competitive advantages of Nitrosospira cluster 3-like AOB over N. viennensis-like AOA in soils under field conditions. Microcosm labeling revealed similar results for active AOA and AOB, although an apparent discrepancy was observed for nitrite-oxidizing bacteria. This study suggests that the soil microbiome represents a relatively stable community resulting from complex evolutionary processes over a large time scale, and microcosms can serve as powerful tools to test the theory of environmental filtering on the key functional microbial guilds.

SUBMITTER: Xia WW

PROVIDER: S-EPMC7657639 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Decomposition of crop residues in soil is mediated by microorganisms whose activities vary with fertilization. The complexity of active microorganisms and their interactions utilizing residues is impossible to disentangle without isotope applications. Thus, 13C-labeled rice residues were employed, and DNA stable-isotope probing (DNA-SIP) combined with high-throughput sequencing was applied to identify microbes active in assimilating residue carbon (C). Manure addition strongly modified microbial community compositions involved in the C flow from rice residues. Relative abundances of the bacterial genus Lysobacter and fungal genus Syncephalis were increased, but abundances of the bacterial genus Streptomyces and fungal genus Trichoderma were decreased in soils receiving mineral fertilizers plus manure (NPKM) compared to levels in soils receiving only mineral fertilizers (NPK). Microbes involved in the flow of residue C formed a more complex network in NPKM than in NPK soils because of the necessity to decompose more diverse organic compounds. The fungal species (Jugulospora rotula and Emericellopsis terricola in NPK and NPKM soils, respectively) were identified as keystone species in the network and may significantly contribute to residue C decomposition. Most of the fungal genera in NPKM soils, especially Chaetomium, Staphylotrichum, Penicillium, and Aspergillus, responded faster to residue addition than those in NPK soils. This is connected with the changes in the composition of the rice residue during degradation and with fungal adaptation (abundance and activity) to continuous manure input. Our findings provide fundamental information about the roles of key microbial groups in residue decomposition and offer important cues on manipulating the soil microbiome for residue utilization and C sequestration in soil.IMPORTANCE Identifying and understanding the active microbial communities and interactions involved in plant residue utilization are key questions to elucidate the transformation of soil organic matter (SOM) in agricultural ecosystems. Microbial community composition responds strongly to management, but little is known about specific microbial groups involved in plant residue utilization and, consequently, microbial functions under different methods of fertilization. We combined DNA stable-isotope (13C) probing and high-throughput sequencing to identify active fungal and bacterial groups degrading residues in soils after 3 years of mineral fertilization with and without manure. Manuring changed the active microbial composition and complexified microbial interactions involved in residue C flow. Most fungal genera, especially Chaetomium, Staphylotrichum, Penicillium, and Aspergillus, responded to residue addition faster in soils that historically had received manure. We generated a valuable library of microorganisms involved in plant residue utilization for future targeted research to exploit specific functions of microbial groups in organic matter utilization and C sequestration.

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Active Soil Nitrifying Communities Revealed by In Situ Transcriptomics and Microcosm-Based Stable-Isotope Probing.

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