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Thrive or survive: prokaryotic life in hypersaline soils

Thrive or survive: prokaryotic life in hypersaline soils
Thrive or survive: prokaryotic life in hypersaline soils
Background: soil services are central to life on the planet, with microorganisms as their main drivers. Thus, the evaluation of soil quality requires an understanding of the principles and factors governing microbial dynamics within it. High salt content is a constraint for life affecting more than 900 million hectares of land, a number predicted to rise at an alarming rate due to changing climate. Nevertheless, little is known about how microbial life unfolds in these habitats. In this study, DNA stable-isotope probing (DNA-SIP) with 18O-water was used to determine for the first time the taxa able to grow in hypersaline soil samples (ECe = 97.02 dS/m). We further evaluated the role of light on prokaryotes growth in this habitat.

Results: we detected growth of both archaea and bacteria, with taxon-specific growth patterns providing insights into the drivers of success in saline soils. Phylotypes related to extreme halophiles, including haloarchaea and Salinibacter, which share an energetically efficient mechanism for salt adaptation (salt-in strategy), dominated the active community. Bacteria related to moderately halophilic and halotolerant taxa, such as Staphylococcus, Aliifodinibius, Bradymonadales or Chitinophagales also grew during the incubations, but they incorporated less heavy isotope. Light did not stimulate prokaryotic photosynthesis but instead restricted the growth of most bacteria and reduced the diversity of archaea that grew.

Conclusions: the results of this study suggest that life in saline soils is energetically expensive and that soil heterogeneity and traits such as exopolysaccharide production or predation may support growth in hypersaline soils. The contribution of phototrophy to supporting the heterotrophic community in saline soils remains unclear. This study paves the way toward a more comprehensive understanding of the functioning of these environments, which is fundamental to their management. Furthermore, it illustrates the potential of further research in saline soils to deepen our understanding of the effect of salinity on microbial communities.
amplicon sequencing, hypersaline environments, prokaryotic communities, saline soil, stable isotope probing
2524-6372
Vera-Gargallo, Blanca
f2dfafeb-e6f0-47cf-a957-ad6567816da6
Hernandez, Marcela
e73477e7-cf3e-4f50-97c8-4494c5b05cd0
Dumont, Marc G.
afd9f08f-bdbb-4cee-b792-1a7f000ee511
Ventosa, Antonio
99bcb3cb-68ec-4558-95be-9999d3ca04eb
Vera-Gargallo, Blanca
f2dfafeb-e6f0-47cf-a957-ad6567816da6
Hernandez, Marcela
e73477e7-cf3e-4f50-97c8-4494c5b05cd0
Dumont, Marc G.
afd9f08f-bdbb-4cee-b792-1a7f000ee511
Ventosa, Antonio
99bcb3cb-68ec-4558-95be-9999d3ca04eb

Vera-Gargallo, Blanca, Hernandez, Marcela, Dumont, Marc G. and Ventosa, Antonio (2023) Thrive or survive: prokaryotic life in hypersaline soils. Environmental Microbiome, 18 (1), [17]. (doi:10.1186/s40793-023-00475-z).

Record type: Article

Abstract

Background: soil services are central to life on the planet, with microorganisms as their main drivers. Thus, the evaluation of soil quality requires an understanding of the principles and factors governing microbial dynamics within it. High salt content is a constraint for life affecting more than 900 million hectares of land, a number predicted to rise at an alarming rate due to changing climate. Nevertheless, little is known about how microbial life unfolds in these habitats. In this study, DNA stable-isotope probing (DNA-SIP) with 18O-water was used to determine for the first time the taxa able to grow in hypersaline soil samples (ECe = 97.02 dS/m). We further evaluated the role of light on prokaryotes growth in this habitat.

Results: we detected growth of both archaea and bacteria, with taxon-specific growth patterns providing insights into the drivers of success in saline soils. Phylotypes related to extreme halophiles, including haloarchaea and Salinibacter, which share an energetically efficient mechanism for salt adaptation (salt-in strategy), dominated the active community. Bacteria related to moderately halophilic and halotolerant taxa, such as Staphylococcus, Aliifodinibius, Bradymonadales or Chitinophagales also grew during the incubations, but they incorporated less heavy isotope. Light did not stimulate prokaryotic photosynthesis but instead restricted the growth of most bacteria and reduced the diversity of archaea that grew.

Conclusions: the results of this study suggest that life in saline soils is energetically expensive and that soil heterogeneity and traits such as exopolysaccharide production or predation may support growth in hypersaline soils. The contribution of phototrophy to supporting the heterotrophic community in saline soils remains unclear. This study paves the way toward a more comprehensive understanding of the functioning of these environments, which is fundamental to their management. Furthermore, it illustrates the potential of further research in saline soils to deepen our understanding of the effect of salinity on microbial communities.

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e-pub ahead of print date: 24 February 2023
Published date: 13 March 2023
Additional Information: Funding Information: This research was supported by grant PID2020-118136 GB-I00 funded by MCIN/AEI/10.13039/501100011033. AV acknowledges support from the Junta de Andalucía (grants P20_01066 and BIO-213), Spain, which included FEDER funds. MGD acknowledges support from the Natural Environment Research Council (NERC, UK). The funding bodies had no role in the design of the study, collection, analysis, and interpretation of data or in writing the manuscript.
Keywords: amplicon sequencing, hypersaline environments, prokaryotic communities, saline soil, stable isotope probing

Identifiers

Local EPrints ID: 480418
URI: http://eprints.soton.ac.uk/id/eprint/480418
ISSN: 2524-6372
PURE UUID: 8c5f61fb-0318-46b4-babb-f59d4e1c05f2
ORCID for Marc G. Dumont: ORCID iD orcid.org/0000-0002-7347-8668

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Date deposited: 02 Aug 2023 16:33
Last modified: 18 Mar 2024 03:33

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Contributors

Author: Blanca Vera-Gargallo
Author: Marcela Hernandez
Author: Marc G. Dumont ORCID iD
Author: Antonio Ventosa

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