Shifts in microbial community composition and metabolism correspond with rapid soil carbon accumulation in response to 20 years of simulated nitrogen deposition
Forsmark, Benjamin ; Bizjak, Tinkara ; Nordin, Annika ; Rosenstock, Nicholas P. LU ; Wallander, Håkan LU
and Gundale, Michael J.
(2024)
In Science of the Total Environment
918.
- Abstract
Anthropogenic nitrogen (N) deposition and fertilization in boreal forests frequently reduces decomposition and soil respiration and enhances C storage in the topsoil. This enhancement of the C sink can be as strong as the aboveground biomass response to N additions and has implications for the global C cycle, but the mechanisms remain elusive. We hypothesized that this effect would be associated with a shift in the microbial community and its activity, and particularly by fungal taxa reported to be capable of lignin degradation and organic N acquisition. We sampled the organic layer below the intact litter of a Norway spruce (Picea abies (L.) Karst) forest in northern Sweden after 20 years of annual N additions at low (12.5 kg N... (More)
Anthropogenic nitrogen (N) deposition and fertilization in boreal forests frequently reduces decomposition and soil respiration and enhances C storage in the topsoil. This enhancement of the C sink can be as strong as the aboveground biomass response to N additions and has implications for the global C cycle, but the mechanisms remain elusive. We hypothesized that this effect would be associated with a shift in the microbial community and its activity, and particularly by fungal taxa reported to be capable of lignin degradation and organic N acquisition. We sampled the organic layer below the intact litter of a Norway spruce (Picea abies (L.) Karst) forest in northern Sweden after 20 years of annual N additions at low (12.5 kg N ha−1 yr−1) and high (50 kg N ha−1 yr−1) rates. We measured microbial biomass using phospholipid fatty-acid analysis (PLFA) and ergosterol measurements and used ITS metagenomics to profile the fungal community of soil and fine-roots. We probed the metabolic activity of the soil community by measuring the activity of extracellular enzymes and evaluated its relationships with the most N responsive soil fungal species. Nitrogen addition decreased the abundance of fungal PLFA markers and changed the fungal community in humus and fine-roots. Specifically, the humus community changed in part due to a shift from Oidiodendron pilicola, Cenococcum geophilum, and Cortinarius caperatus to Tylospora fibrillosa and Russula griseascens. These microbial community changes were associated with decreased activity of Mn-peroxidase and peptidase, and an increase in the activity of C acquiring enzymes. Our results show that the rapid accumulation of C in the humus layer frequently observed in areas with high N deposition is consistent with a shift in microbial metabolism, where decomposition associated with organic N acquisition is downregulated when inorganic N forms are readily available.
(Less)
- author
- Forsmark, Benjamin
; Bizjak, Tinkara
; Nordin, Annika
; Rosenstock, Nicholas P.
LU
; Wallander, Håkan
LU
and Gundale, Michael J.
- organization
- publishing date
- 2024-03
- type
- Contribution to journal
- publication status
- published
- subject
- keywords
- Boreal forest, Carbon sequestration, Ectomycorrhizal fungi, Extracellular enzymes, Microbial community, Nitrogen deposition
- in
- Science of the Total Environment
- volume
- 918
- article number
- 170741
- pages
- 13 pages
- publisher
- Elsevier
- external identifiers
-
- pmid:38325494
- scopus:85184838251
- ISSN
- 0048-9697
- DOI
- 10.1016/j.scitotenv.2024.170741
- language
- English
- LU publication?
- yes
- id
- e36c5183-1cf2-4990-9020-cc783309b112
- date added to LUP
- 2024-03-06 13:40:56
- date last changed
- 2024-04-18 14:30:12
@article{e36c5183-1cf2-4990-9020-cc783309b112,
abstract = {{<p>Anthropogenic nitrogen (N) deposition and fertilization in boreal forests frequently reduces decomposition and soil respiration and enhances C storage in the topsoil. This enhancement of the C sink can be as strong as the aboveground biomass response to N additions and has implications for the global C cycle, but the mechanisms remain elusive. We hypothesized that this effect would be associated with a shift in the microbial community and its activity, and particularly by fungal taxa reported to be capable of lignin degradation and organic N acquisition. We sampled the organic layer below the intact litter of a Norway spruce (Picea abies (L.) Karst) forest in northern Sweden after 20 years of annual N additions at low (12.5 kg N ha<sup>−1</sup> yr<sup>−1</sup>) and high (50 kg N ha<sup>−1</sup> yr<sup>−1</sup>) rates. We measured microbial biomass using phospholipid fatty-acid analysis (PLFA) and ergosterol measurements and used ITS metagenomics to profile the fungal community of soil and fine-roots. We probed the metabolic activity of the soil community by measuring the activity of extracellular enzymes and evaluated its relationships with the most N responsive soil fungal species. Nitrogen addition decreased the abundance of fungal PLFA markers and changed the fungal community in humus and fine-roots. Specifically, the humus community changed in part due to a shift from Oidiodendron pilicola, Cenococcum geophilum, and Cortinarius caperatus to Tylospora fibrillosa and Russula griseascens. These microbial community changes were associated with decreased activity of Mn-peroxidase and peptidase, and an increase in the activity of C acquiring enzymes. Our results show that the rapid accumulation of C in the humus layer frequently observed in areas with high N deposition is consistent with a shift in microbial metabolism, where decomposition associated with organic N acquisition is downregulated when inorganic N forms are readily available.</p>}},
author = {{Forsmark, Benjamin and Bizjak, Tinkara and Nordin, Annika and Rosenstock, Nicholas P. and Wallander, Håkan and Gundale, Michael J.}},
issn = {{0048-9697}},
keywords = {{Boreal forest; Carbon sequestration; Ectomycorrhizal fungi; Extracellular enzymes; Microbial community; Nitrogen deposition}},
language = {{eng}},
publisher = {{Elsevier}},
series = {{Science of the Total Environment}},
title = {{Shifts in microbial community composition and metabolism correspond with rapid soil carbon accumulation in response to 20 years of simulated nitrogen deposition}},
url = {{http://dx.doi.org/10.1016/j.scitotenv.2024.170741}},
doi = {{10.1016/j.scitotenv.2024.170741}},
volume = {{918}},
year = {{2024}},
}