Extracellular enzyme ratios reveal locality and horizon-specific carbon, nitrogen, and phosphorus limitations in Arctic permafrost soils

Varsadiya, Milan; Liebmann, Patrick; Petters, Sebastian; Hugelius, Gustaf; Urich, Tim; Guggenberger, Georg; Bárta, Jiří

doi:10.1007/s10533-022-00967-z

Cited by 7 publications

(5 citation statements)

References 58 publications

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“…Methanogenesis in particular is responsible for fluxes of methane in warming tundra ( 132 , 134 , 135 ) and was associated with tundra in the current study. Additionally, a gene involved in nitric oxide cycling (PF08768) ( 136 – 138 ), as well as a variety of anaerobic organisms and P-related genes (K03525, K00997, K00992, K13497, and PF08009) ( 139 – 141 ), also provide insight into the molecular functions of tundra in the context of global climate change. Interestingly, we also found evidence for pathogen resistance within the tundra genomic fingerprint (PF11203, PF05045), lending credence to a small number of recent studies suggesting permafrost environments as one of the largest reservoirs of soil viruses ( 142 – 145 ) and a possible linkage between soil methane and viral infection ( 146 ).…”

Section: Discussionmentioning

confidence: 99%

Genomic fingerprints of the world’s soil ecosystems

Graham,

Garayburu-Caruso,

et al. 2024

mSystems

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Despite the explosion of soil metagenomic data, we lack a synthesized understanding of patterns in the distribution and functions of soil microorganisms. These patterns are critical to predictions of soil microbiome responses to climate change and resulting feedbacks that regulate greenhouse gas release from soils. To address this gap, we assay 1,512 manually curated soil metagenomes using complementary annotation databases, read-based taxonomy, and machine learning to extract multidimensional genomic fingerprints of global soil microbiomes. Our objective is to uncover novel biogeographical patterns of soil microbiomes across environmental factors and ecological biomes with high molecular resolution. We reveal shifts in the potential for (i) microbial nutrient acquisition across pH gradients; (ii) stress-, transport-, and redox-based processes across changes in soil bulk density; and (iii) greenhouse gas emissions across biomes. We also use an unsupervised approach to reveal a collection of soils with distinct genomic signatures, characterized by coordinated changes in soil organic carbon, nitrogen, and cation exchange capacity and in bulk density and clay content that may ultimately reflect soil environments with high microbial activity. Genomic fingerprints for these soils highlight the importance of resource scavenging, plant-microbe interactions, fungi, and heterotrophic metabolisms. Across all analyses, we observed phylogenetic coherence in soil microbiomes—more closely related microorganisms tended to move congruently in response to soil factors. Collectively, the genomic fingerprints uncovered here present a basis for global patterns in the microbial mechanisms underlying soil biogeochemistry and help beget tractable microbial reaction networks for incorporation into process-based models of soil carbon and nutrient cycling. IMPORTANCE We address a critical gap in our understanding of soil microorganisms and their functions, which have a profound impact on our environment. We analyzed 1,512 global soils with advanced analytics to create detailed genetic profiles (fingerprints) of soil microbiomes. Our work reveals novel patterns in how microorganisms are distributed across different soil environments. For instance, we discovered shifts in microbial potential to acquire nutrients in relation to soil acidity, as well as changes in stress responses and potential greenhouse gas emissions linked to soil structure. We also identified soils with putative high activity that had unique genomic characteristics surrounding resource acquisition, plant-microbe interactions, and fungal activity. Finally, we observed that closely related microorganisms tend to respond in similar ways to changes in their surroundings. Our work is a significant step toward comprehending the intricate world of soil microorganisms and its role in the global climate.

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Section: Discussionmentioning

confidence: 99%

Genomic fingerprints of the world’s soil ecosystems

Graham,

Garayburu-Caruso,

et al. 2024

mSystems

View full text Add to dashboard Cite

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“…Microbial P limitation has rarely been reported in studies of Arctic or subarctic ecosystems (Varsadiya et al, 2022). Previous assessments using combined N, P, and potassium (K) addition highlighted the possibility that microorganisms in subarctic soils could be nutrient‐limited (Rinnan et al, 2007; Ruess et al, 1999) and, although microbial P limitation was offered as an interpretation (Rinnan et al, 2007), these studies lacked the ability to distinguish between limitation by N, P, or K. Here, we were able to refine the microbial growth limitation assessment by identifying P as the secondary limiting factor (Figure 1a).…”

Section: Discussionmentioning

confidence: 99%

“…The greater abundance of shrubs may result in both a higher uptake of N from soil by plants and a higher plant-derived C input to soil, which might alleviate C limitation and intensify N limitation for soil microorganisms in the Alaskan tundra. Microbial P limitation has rarely been reported in studies of Arctic or subarctic ecosystems (Varsadiya et al, 2022). Previous assessments using combined N, P, and potassium (K) addition highlighted the possibility that microorganisms in subarctic soils could be nutrient-limited (Rinnan et al, 2007;Ruess et al, 1999) and, although microbial P T A B L E 2 Bacterial growth, fungal growth, respiration, fungal-to-bacterial growth ratio, and carbon use efficiency in soils from different field-treatments.…”

Section: Resource Limitations For Microbial Growthmentioning

confidence: 99%

Limiting resources for soil microbial growth in climate change simulation treatments in the subarctic

Yuan,

Na,

Hicks

et al. 2023

Ecology

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The microbial use of resources to sustain life and reproduce influences for example, decomposition and plant nutrient provisioning. The study of “limiting factors” has shed light on the interaction between plants and their environment. Here, we investigated whether carbon (C), nitrogen (N), or phosphorus (P) was limiting for soil microorganisms in a subarctic tundra heath, and how changes in resource availability associated with climate change affected this. We studied samples in which changes in resource availability due to climate warming were simulated by the addition of birch litter and/or inorganic N. To these soils, we supplied factorial C (as glucose), N (as NH4NO3), and P (as KH2PO4/K2HPO4) additions (“limiting factor assays,” LFA), to determine the limiting factors. The combination of C and P induced large growth responses in all soils and, combined with a systematic tendency for growth increases by C, this suggested that total microbial growth was primarily limited by C and secondarily by P. The C limitation was alleviated by the field litter treatment and strengthened by N fertilization. The microbial growth response to the LFA‐C and LFA‐P addition was strongest in the field‐treatment that combined litter and N addition. We also found that bacteria were closer to P limitation than fungi. Our results suggest that, under a climate change scenario, increased C availability resulting from Arctic greening, treeline advance, and shrubification will reduce the microbial C limitation, while increased N availability resulting from warming will intensify the microbial C limitation. Our results also suggest that the synchronous increase of both C and N availability might lead to a progressive P limitation of microbial growth, primarily driven by bacteria being closer to P limitation. These shifts in microbial resource limitation might lead to a microbial targeting of the limiting element from organic matter, and also trigger competition for nutrients between plants and microorganisms, thus modulating the productivity of the ecosystem.

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“…Methanogenesis in particular is responsible for fluxes of methane in warming tundra (131, 133, 134) and was associated with tundra in the current study. Additionally, a gene involved in nitric oxide cycling (PF08768) (135–137), as well as a variety of anaerobic organisms and P-related genes (K03525, K00997, K00992, K13497, PF08009) (138–140), also provide insight into the molecular functions of tundra in the context of global climate change. Interestingly, we also found evidence for pathogen resistance within the tundra genomic signature (PF11203, PF05045), lending credence to a small number of recent studies suggesting permafrost environments as one of the largest reservoirs of soil viruses (141–144) and a possible linkage between soil methane and viral infection (145).…”

Section: Discussionmentioning

confidence: 99%

Section: Soil Genomic Potential For Greenhouse Gas Emissions Differs ...mentioning

confidence: 99%

Genomic fingerprints of the world’s soil ecosystems

Graham,

Garayburu-Caruso,

et al. 2023

Preprint

View full text Add to dashboard Cite

Despite the explosion of soil metagenomic data, we lack a synthesized understanding of patterns in the distribution and functions of soil microorganisms. These patterns are critical to predictions of soil microbiome responses to climate change and resulting feedbacks that regulate greenhouse gas release from soils. To address this gap, we assayed 1512 manually-curated soil metagenomes using complementary annotation databases, read-based taxonomy, and machine learning to extract multidimensional genomic fingerprints of global soil microbiomes. We reveal novel biogeographical patterns of soil microbiomes across environmental factors and ecological biomes with high molecular resolution. Specifically, we demonstrate shifts in the potential for microbial nutrient acquisition across pH gradients; for stress, transport, and redox-based processes across changes in soil bulk density; and for greenhouse gas emissions across biomes. We also use an unsupervised approach to reveal a collection of soils with distinct genomic signatures, characterized by coordinated changes in soil organic carbon, nitrogen, and cation exchange capacity and in bulk density and clay content that may ultimately reflect soil environments with high microbial activity. Genomic fingerprints for these soils highlight the importance of resource scavenging, plant-microbe interactions, fungi, and heterotrophic metabolisms. Across all analyses, we observed phylogenetic coherence in soil microbiomes –– more closely related microorganisms tended to move congruently in response to soil factors. Collectively, the genomic fingerprints uncovered here present a basis for global patterns in the microbial mechanisms underlying soil biogeochemistry and help beget tractable microbial reaction networks for incorporation into process-based models of soil carbon and nutrient cycling.ImportanceWe address a critical gap in our understanding of soil microorganisms and their functions, which have a profound impact on our environment. We analyzed 1512 global soils with advanced analytics to create detailed genetic profiles (fingerprints) of soil microbiomes. This reveals novel patterns in how these microorganisms are distributed across different soil environments. For instance, we discovered shifts in their potential to acquire nutrients in relation to soil acidity, as well as changes in stress responses and potential greenhouse gas emissions linked to soil density. We also identified soils with putative high activity that had unique genomic characteristics surrounding resource acquisition, plant-microbe interactions, and fungal activity. Finally, we observed that closely related microorganisms tend to respond in similar ways to changes in their surroundings. Our work is a significant step towards comprehending the intricate world of soil microorganisms and its role in the global climate.

show abstract

Extracellular enzyme ratios reveal locality and horizon-specific carbon, nitrogen, and phosphorus limitations in Arctic permafrost soils

Cited by 7 publications

References 58 publications

Genomic fingerprints of the world’s soil ecosystems

Genomic fingerprints of the world’s soil ecosystems

Limiting resources for soil microbial growth in climate change simulation treatments in the subarctic

Genomic fingerprints of the world’s soil ecosystems

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