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Microbial life deep underground: From anaerobic cultures to reconstructed genomes
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Systems Biology of Microorganisms)ORCID iD: 0000-0002-5529-2237
2024 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The deep biosphere refers to the vast ecosystem of life beneath the Earth’s surface, residing in the fractured bedrock and pores of rocks, largely isolated from solar energy. These fractures enclose an important reservoir of groundwater that contains microorganisms active in processes such as the uptake of inorganic carbon, sulfur cycling, or the degradation of organic matter. However, there is still much knowledge to be gained on the diversity and function of these subsurface microorganisms, and how the surface influences subsurface life. In this work, I explored interactions among subsurface microorganisms, studied subsurface microbial diversity in the light of surface recharge, and characterized microbial populations residing in biofilms.

Potential interactions among microorganisms were explored with anaerobic cultures using groundwaters from the Äspö Hard Rock Laboratory. By removal of larger cells (> 0.45 𝜇m in diameter), an inoculum enriched in ultra-small bacteria (nanobacteria) was obtained. Despite the presence of various sources of energy and nutrients, these nanobacteria did not grow over prolonged incubation times up to four months. Reconstructed genomes confirmed this group of bacteria to have a low metabolic potential, indicative of a symbiotic lifestyle.

Characterization of microbial communities in subsurface groundwaters and overlying environments on Äspö island revealed that a substantial proportion of the subsurface community was also detected in soil-hosted groundwaters. Considering the unidirectional water flow, this showed that part of the subsurface diversity between 70 and 460 m depth could originate from surface recharge, especially for the shallower groundwaters. In contrast to the high microbial diversity observed in Äspö groundwaters, characterization of a fracture fluid at 975 m depth in central Sweden revealed a microbial community dominated by a single population, adapted to the energy-limited conditions in the deep subsurface, namely the bacterium Candidatus Desulforudis audaxviator.

Furthermore, the activity (based on RNA transcripts) of attached microbial populations was measured using flow-cells that facilitated biofilm formation. An elevated number of genes involved in the transition from a planktonic to an attached lifestyle was observed. Interestingly, comparing the microbial activity in the biofilm to the planktonic community revealed Thiobacillus denitrificans to have a principal role in the biofilm formation. Combined, these findings help understand the magnitude of microbial diversity in the continental subsurface as well as how these microorganisms are adapted to cope with the energy limitations in this subsurface ecosystem.

Place, publisher, year, edition, pages
Linnaeus University Press, 2024. , p. 51
Series
Linnaeus University Dissertations ; 516
Keywords [en]
Continental deep biosphere, microbial ecology, anaerobic enrichment cultures, Candidatus Desulforudis audaxviator, Thiobacillus denitrificans, flow-cells
National Category
Bioinformatics and Systems Biology
Research subject
Ecology, Microbiology; Natural Science, Ecology
Identifiers
URN: urn:nbn:se:lnu:diva-126378DOI: 10.15626/LUD.516.2023ISBN: 9789180821209 (print)ISBN: 9789180821216 (electronic)OAI: oai:DiVA.org:lnu-126378DiVA, id: diva2:1826328
Public defence
2024-02-16, Azur, Hus Vita, Kalmar, 09:00 (English)
Opponent
Supervisors
Available from: 2024-01-11 Created: 2024-01-11 Last updated: 2024-01-23Bibliographically approved
List of papers
1. Connectivity of Fennoscandian Shield terrestrial deep biosphere microbiomes with surface communities
Open this publication in new window or tab >>Connectivity of Fennoscandian Shield terrestrial deep biosphere microbiomes with surface communities
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2022 (English)In: Communications Biology, E-ISSN 2399-3642, Vol. 5, no 1, article id 37Article in journal (Refereed) Published
Abstract [en]

The deep biosphere is an energy constrained ecosystem yet fosters diverse microbial communities that are key in biogeochemical cycling. Whether microbial communities in deep biosphere groundwaters are shaped by infiltration of allochthonous surface microorganisms or the evolution of autochthonous species remains unresolved. In this study, 16S rRNA gene amplicon analyses showed that few groups of surface microbes infiltrated deep biosphere groundwaters at the Äspö Hard Rock Laboratory, Sweden, but that such populations constituted up to 49% of the microbial abundance. The dominant persisting phyla included Patescibacteria, Proteobacteria, and Epsilonbacteraeota. Despite the hydrological connection of the Baltic Sea with the studied groundwaters, infiltrating microbes predominantly originated from deep soil groundwater. Most deep biosphere groundwater populations lacked surface representatives, suggesting that they have evolved from ancient autochthonous populations. We propose that deep biosphere groundwater communities in the Fennoscandian Shield consist of selected infiltrated and indigenous populations adapted to the prevailing conditions.

Place, publisher, year, edition, pages
Nature Publishing Group, 2022
National Category
Microbiology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-109214 (URN)10.1038/s42003-021-02980-8 (DOI)000741646700012 ()35017653 (PubMedID)2-s2.0-85122794173 (Scopus ID)2022 (Local ID)2022 (Archive number)2022 (OAI)
Funder
Swedish Research Council, 2018-04311
Available from: 2022-01-14 Created: 2022-01-14 Last updated: 2024-01-11Bibliographically approved
2. Thiobacillus as a key player for biofilm formation in oligotrophic groundwaters of the Fennoscandian Shield
Open this publication in new window or tab >>Thiobacillus as a key player for biofilm formation in oligotrophic groundwaters of the Fennoscandian Shield
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2023 (English)In: npj Biofilms and Microbiomes, E-ISSN 2055-5008, Vol. 9, no 1, article id 41Article in journal (Refereed) Published
Abstract [en]

Biofilm formation is a common adaptation for microbes in energy-limited conditions such as those prevalent in the vast deep terrestrial biosphere. However, due to the low biomass and the inaccessible nature of subsurface groundwaters, the microbial populations and genes involved in its formation are understudied. Here, a flow-cell system was designed to investigate biofilm formation under in situ conditions in two groundwaters of contrasting age and geochemistry at the aspo Hard Rock Laboratory, Sweden. Metatranscriptomes showed Thiobacillus, Sideroxydans, and Desulforegula to be abundant and together accounted for 31% of the transcripts in the biofilm communities. Differential expression analysis highlighted Thiobacillus to have a principal role in biofilm formation in these oligotrophic groundwaters by being involved in relevant processes such as the formation of extracellular matrix, quorum sensing, and cell motility. The findings revealed an active biofilm community with sulfur cycling as a prominent mode of energy conservation in the deep biosphere.

Place, publisher, year, edition, pages
Nature Publishing Group, 2023
National Category
Microbiology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-123554 (URN)10.1038/s41522-023-00408-1 (DOI)001012841200001 ()37349512 (PubMedID)2-s2.0-85162813078 (Scopus ID)
Available from: 2023-08-10 Created: 2023-08-10 Last updated: 2024-01-11Bibliographically approved

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Westmeijer, George

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