Transcriptomic responses to warming and cooling of an Arctic tundra soil microbiome

Schostag, Morten; Anwar, Muhammad Zohaib; Jacobsen, Carsten Suhr; Larose, Catherine; Vogel, Timothy M.; Maccario, Lorrie; Jacquiod, Samuel; Faucherre, Samuel; Priemé, Anders

doi:10.1101/599233

Cited by 3 publications

(6 citation statements)

References 110 publications

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“…A pronounced shift during the incubation period was noticed by Schostag et al. [14] that was not replicated by the assembly-free approach. However, using CoMW, we identified an increase of genes in the subsystem “[P] Inorganic ion transport and metabolism.” During cooling, CoMW also captured the upregulation and downregulation of genes related to “[J] Translation, ribosomal structure, and biogenesis” and “[C] Energy production and conversion,” respectively (Fig.…”

Section: Resultsmentioning

confidence: 89%

“…Three different protein databases were selected for this benchmarking in order to include a representative selection of 3 different degrees of specialization, on a range from a more inclusive database with wide coverage (universality) and low degree of expert curation to a smaller, highly curated database, with more narrow coverage: (i) M5nr [11], an inclusive and comprehensive non-redundant protein database in combination with Evolutionary Genealogy of Genes: Non-supervised Orthologous Groups (eggNOG) hierarchical annotation; (ii) Carbohydrate-Active Enzymes (CAZy) [12], a database dedicated to describing the families of structurally related catalytic and carbohydrate-binding modules of enzymes; and (iii) Nitrogen Cycling Database (NCycDB) [13], a specialized and manually curated database covering only nitrogen cycle genes. Finally, to estimate the consistency and variance in the results caused by the choice of approach, we then applied them to real-world metatranscriptomes from microbial communities in (i) active-layer permafrost soil from Svalbard, Norway [14], and (ii) ash-impacted Danish forest soil [15].…”

Section: Introductionmentioning

confidence: 99%

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To assemble or not to resemble—A validated Comparative Metatranscriptomics Workflow (CoMW)

et al. 2019

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Background Metatranscriptomics has been used widely for investigation and quantification of microbial communities’ activity in response to external stimuli. By assessing the genes expressed, metatranscriptomics provides an understanding of the interactions between different major functional guilds and the environment. Here, we present a de novo assembly-based Comparative Metatranscriptomics Workflow (CoMW) implemented in a modular, reproducible structure. Metatranscriptomics typically uses short sequence reads, which can either be directly aligned to external reference databases (“assembly-free approach”) or first assembled into contigs before alignment (“assembly-based approach”). We also compare CoMW (assembly-based implementation) with an assembly-free alternative workflow, using simulated and real-world metatranscriptomes from Arctic and temperate terrestrial environments. We evaluate their accuracy in precision and recall using generic and specialized hierarchical protein databases. Results CoMW provided significantly fewer false-positive results, resulting in more precise identification and quantification of functional genes in metatranscriptomes. Using the comprehensive database M5nr, the assembly-based approach identified genes with only 0.6% false-positive results at thresholds ranging from inclusive to stringent compared with the assembly-free approach, which yielded up to 15% false-positive results. Using specialized databases (carbohydrate-active enzyme and nitrogen cycle), the assembly-based approach identified and quantified genes with 3–5 times fewer false-positive results. We also evaluated the impact of both approaches on real-world datasets. Conclusions We present an open source de novo assembly-based CoMW. Our benchmarking findings support assembling short reads into contigs before alignment to a reference database because this provides higher precision and minimizes false-positive results.

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Section: Resultsmentioning

confidence: 89%

Section: Introductionmentioning

confidence: 99%

To assemble or not to resemble—A validated Comparative Metatranscriptomics Workflow (CoMW)

et al. 2019

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“…The recycling of cell wall components such as peptidoglycan from microbial necromass by microbes has been recognized as an important C and N source in soil (Basler et al, 2015;Guenet et al, 2011;Hu et al, 2017;Kindler et al, 2006). In addition, various studies have previously stressed the importance of C and nutrient release from vulnerable cells as energy and nutrient sources upon stressful stimuli like heat, radiation and freezethaw transitions (Mooshammer et al, 2017;Perez-Mon et al, 2020;Schostag, Anwar, et al, 2019;. Similar to the general functional annotation with eggNOG, genes within each CAZy family reacted very inconsistently, and highly increased genes were affiliated with a few abundant genera (Phenylobacterium, Caulobacter, Ralstonia and Dyella) that have previously been found to respond positively to high temperature (Donhauser et al, 2020;Jurburg, Nunes, Brejnrod, et al, 2017;Jurburg, Nunes, Stegen, et al, 2017).…”

Section: Changes In the Microbial C-cycling Potentialmentioning

confidence: 85%

High temperatures enhance the microbial genetic potential to recycle C and N from necromass in high‐mountain soils

Donhauser

Bergk-Pinto

et al. 2021

Global Change Biology

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Climate change is strongly affecting high‐mountain soils and warming in particular is associated with pronounced changes in microbe‐mediated C and N cycling, affecting plant‐soil interactions and greenhouse gas balances and therefore feedbacks to global warming. We used shotgun metagenomics to assess changes in microbial community structures, as well as changes in microbial C‐ and N‐cycling potential and stress response genes and we linked these data with changes in soil C and N pools and temperature‐dependent measurements of bacterial growth rates. We did so by incubating high‐elevation soil from the Swiss Alps at 4°C, 15°C, 25°C, or 35°C for 1 month. We found no shift with increasing temperature in the C‐substrate‐degrader community towards taxa more capable of degrading recalcitrant organic matter. Conversely, at 35°C, we found an increase in genes associated with the degradation and modification of microbial cell walls, together with high bacterial growth rates. Together, these findings suggest that the rapidly growing high‐temperature community is fueled by necromass from heat‐sensitive taxa. This interpretation was further supported by a shift in the microbial N‐cycling potential towards N mineralization and assimilation under higher temperatures, along with reduced potential for conversions among inorganic N forms. Microbial stress‐response genes reacted inconsistently to increasing temperature, suggesting that the high‐temperature community was not severely stressed by these conditions. Rather, soil microbes were able to acclimate by changing the thermal properties of membranes and cell walls as indicated by an increase in genes involved in membrane and cell wall modifications as well as a shift in the optimum temperature for bacterial growth towards the treatment temperature. Overall, our results suggest that high temperatures, as they may occur with heat waves under global warming, promote a highly active microbial community capable of rapid mineralization of microbial necromass, which may transiently amplify warming effects.

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“…The aim of the study was to understand taxonomic and functional shifts in microbial communities caused by climate change in the Arctic. A pronounced shift during the incubation period was noticed by Schostag et al [14] which was not replicated by the assembly-free approach. However, using CoMW, we identified an increase of genes in the subsystem “[P] Inorganic ion transport and metabolism”.…”

Section: Resultsmentioning

confidence: 87%

“…Three different protein databases were selected for this benchmarking in order to include a representative selection of three different degrees of specialization, on a range from a more inclusive database with wide coverage (universality) and low degree of expert curation, to a smaller, highly curated database, with more narrow coverage: 1) M5nr [11] an inclusive and comprehensive non-redundant protein database in combination with eggNOG hierarchical annotation 2) Carbohydrate-Active Enzymes (CAZymes) [12] a database dedicated to describing the families of structurally-related catalytic and carbohydrate-binding modules of enzymes and 3) Nitrogen Cycling Database (NCycDB) [13] a specialized and manually curated database covering only N cycle genes. Finally, in order to estimate the consistency and variance in the results caused by the choice of approach we then applied them to real world metatranscriptomes from microbial communities in 1) active-layer permafrost soil from Svalbard [14] and 2) Ash impacted Danish Forest soil [15].…”

Section: Introductionmentioning

confidence: 99%

To assemble or not to resemble – A validated Comparative Metatranscriptomics Workflow (CoMW)

Anwar

Lanzén

Bang‐Andreasen

et al. 2019

Preprint

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BackgroundMetatranscriptomics has been used widely for investigation and quantification of microbial communities’ activity in response to external stimuli. By assessing the genes expressed, metatranscriptomics provide an understanding of the interactions between different major functional guilds and the environment. Here, we present de-novo assembly-based Comparative Metatranscriptomics Workflow (CoMW) implemented in a modular, reproducible structure, significantly improving the annotation and quantification of metatranscriptomes. Metatranscriptomics typically utilize short sequence reads, which can either be directly aligned to external reference databases (“assembly-free approach”) or first assembled into contigs before alignment (“assembly-based approach”). We also compare CoMW (assembly-based implementation) with assembly-free alternative workflow, using simulated and real-world metatranscriptomes from Arctic and Temperate terrestrial environments. We evaluate their accuracy in precision and recall using generic and specialized hierarchical protein databases.ResultsCoMW provided significantly fewer false positives resulting in more precise identification and quantification of functional genes in metatranscriptomes. Using the comprehensive database M5nr, the assembly-based approach identified genes with only 0.6% false positives at thresholds ranging from inclusive to stringent compared to the assembly-free approach yielding up to 15% false positives. Using specialized databases (Carbohydrate Active-enzyme and Nitrogen Cycle), the assembly-based approach identified and quantified genes with 3-5x less false positives. We also evaluated the impact of both approaches on real-world datasets.ConclusionsWe present an open source de-novo assembly-based Comparative Metatranscriptomics Workflow (CoMW). Our benchmarking findings support the argument of assembling short reads into contigs before alignment to a reference database, since this provides higher precision and minimizes false positives.

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Transcriptomic responses to warming and cooling of an Arctic tundra soil microbiome

Abstract: 6Background: Arctic surface soils experience pronounced seasonal changes in temperature

Cited by 3 publications

References 110 publications

To assemble or not to resemble—A validated Comparative Metatranscriptomics Workflow (CoMW)

To assemble or not to resemble—A validated Comparative Metatranscriptomics Workflow (CoMW)

High temperatures enhance the microbial genetic potential to recycle C and N from necromass in high‐mountain soils

To assemble or not to resemble – A validated Comparative Metatranscriptomics Workflow (CoMW)

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