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Rewetting the hyper-arid Atacama Desert soil reactivates a carbon-starved microbial decomposer community and also triggers archaeal metabolism

Rosinger, Christoph LU ; Rousk, Johannes LU ; Bonkowski, Michael ; Rethemeyer, Janet and Jaeschke, Andrea (2023) In Science of the Total Environment 892.
Abstract

Extreme environmental conditions make soils of the hyper-arid Atacama Desert one of the most hostile habitats for life on the planet. During the short intervals of moisture availability that occur, it remains unresolved how soil microorganisms physiologically respond to such dramatic environmental changes. Therefore, we simulated a precipitation event – without (H2O) and with (H2O + C) labile carbon (C) supplementation – and investigated the responses in microbial communities (using phospholipid fatty acids (PLFAs) and archaeal glycerol dialkyl glycerol tetraether (GDGTs)) and physiology (by means of respiration, bacterial and fungal growth and C-use efficiency (CUE)) during a five-day incubation. We demonstrated... (More)

Extreme environmental conditions make soils of the hyper-arid Atacama Desert one of the most hostile habitats for life on the planet. During the short intervals of moisture availability that occur, it remains unresolved how soil microorganisms physiologically respond to such dramatic environmental changes. Therefore, we simulated a precipitation event – without (H2O) and with (H2O + C) labile carbon (C) supplementation – and investigated the responses in microbial communities (using phospholipid fatty acids (PLFAs) and archaeal glycerol dialkyl glycerol tetraether (GDGTs)) and physiology (by means of respiration, bacterial and fungal growth and C-use efficiency (CUE)) during a five-day incubation. We demonstrated that bacterial and fungal growth does occur in these extreme soils following rewetting, albeit at 100–10,000-fold lower rates compared to previously studied soil systems. C supplementation increased levels of bacterial growth and respiration responses by 5- and 50-fold, respectively, demonstrating a C-limited microbial decomposer community. While the microbial CUE following rewetting was c. 14 %, the addition of labile C during rewetting resulted in a substantial reduction (c. 1.6 %). Consistent with these interpretations, the PLFA composition clearly shifted from saturated towards more unsaturated and branched PLFAs, which could arise from (i) a physiological adaptation of the cell membrane to changing osmotic conditions or (ii) a community composition shift. Significant increases in total PLFA concentrations were solely found with H2O + C addition. Contrary to other recent studies, we found evidence for a metabolically active archaeal community in these hyper-arid soils upon rewetting. We conclude that (i) microorganisms in this extreme soil habitat can be activated and grow within days following rewetting, (ii) available C is the limiting factor for microbial growth and biomass gains, and (iii) that an optimization of tolerating the extreme conditions while maintaining a high CUE comes at the expense of very poor resource-use efficiency during high resource availability.

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author
; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Atacama Desert, Hyper-arid soils, Nutrient limitation, Physiological adaptation, Rewetting, Soil microbial growth
in
Science of the Total Environment
volume
892
article number
164785
publisher
Elsevier
external identifiers
  • pmid:37302588
  • scopus:85162121969
ISSN
0048-9697
DOI
10.1016/j.scitotenv.2023.164785
language
English
LU publication?
yes
id
6b41ac76-fe30-4830-86e6-c8d10d82227e
date added to LUP
2023-08-30 14:21:38
date last changed
2024-04-20 02:14:06
@article{6b41ac76-fe30-4830-86e6-c8d10d82227e,
  abstract     = {{<p>Extreme environmental conditions make soils of the hyper-arid Atacama Desert one of the most hostile habitats for life on the planet. During the short intervals of moisture availability that occur, it remains unresolved how soil microorganisms physiologically respond to such dramatic environmental changes. Therefore, we simulated a precipitation event – without (H<sub>2</sub>O) and with (H<sub>2</sub>O + C) labile carbon (C) supplementation – and investigated the responses in microbial communities (using phospholipid fatty acids (PLFAs) and archaeal glycerol dialkyl glycerol tetraether (GDGTs)) and physiology (by means of respiration, bacterial and fungal growth and C-use efficiency (CUE)) during a five-day incubation. We demonstrated that bacterial and fungal growth does occur in these extreme soils following rewetting, albeit at 100–10,000-fold lower rates compared to previously studied soil systems. C supplementation increased levels of bacterial growth and respiration responses by 5- and 50-fold, respectively, demonstrating a C-limited microbial decomposer community. While the microbial CUE following rewetting was c. 14 %, the addition of labile C during rewetting resulted in a substantial reduction (c. 1.6 %). Consistent with these interpretations, the PLFA composition clearly shifted from saturated towards more unsaturated and branched PLFAs, which could arise from (i) a physiological adaptation of the cell membrane to changing osmotic conditions or (ii) a community composition shift. Significant increases in total PLFA concentrations were solely found with H<sub>2</sub>O + C addition. Contrary to other recent studies, we found evidence for a metabolically active archaeal community in these hyper-arid soils upon rewetting. We conclude that (i) microorganisms in this extreme soil habitat can be activated and grow within days following rewetting, (ii) available C is the limiting factor for microbial growth and biomass gains, and (iii) that an optimization of tolerating the extreme conditions while maintaining a high CUE comes at the expense of very poor resource-use efficiency during high resource availability.</p>}},
  author       = {{Rosinger, Christoph and Rousk, Johannes and Bonkowski, Michael and Rethemeyer, Janet and Jaeschke, Andrea}},
  issn         = {{0048-9697}},
  keywords     = {{Atacama Desert; Hyper-arid soils; Nutrient limitation; Physiological adaptation; Rewetting; Soil microbial growth}},
  language     = {{eng}},
  publisher    = {{Elsevier}},
  series       = {{Science of the Total Environment}},
  title        = {{Rewetting the hyper-arid Atacama Desert soil reactivates a carbon-starved microbial decomposer community and also triggers archaeal metabolism}},
  url          = {{http://dx.doi.org/10.1016/j.scitotenv.2023.164785}},
  doi          = {{10.1016/j.scitotenv.2023.164785}},
  volume       = {{892}},
  year         = {{2023}},
}