Biomineralization in Cave Bacteria—Popcorn and Soda Straw Crystal Formations, Morphologies, and Potential Metabolic Pathways
Caves are extreme, often oligotrophic, environments that house diverse groups of microorganisms. Many of these microbes can perform microbiologically induced carbonate precipitation (MICP) to form crystalline secondary cave deposits known as speleothems. The urease family is a group of enzymes invol...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-07-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.933388/full |
| _version_ | 1811327492669046784 |
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| author | Keegan Koning Richenda McFarlane Jessica T. Gosse Sara Lawrence Lynnea Carr Derrick Horne Nancy Van Wagoner Christopher N. Boddy Naowarat Cheeptham |
| author_facet | Keegan Koning Richenda McFarlane Jessica T. Gosse Sara Lawrence Lynnea Carr Derrick Horne Nancy Van Wagoner Christopher N. Boddy Naowarat Cheeptham |
| author_sort | Keegan Koning |
| collection | DOAJ |
| description | Caves are extreme, often oligotrophic, environments that house diverse groups of microorganisms. Many of these microbes can perform microbiologically induced carbonate precipitation (MICP) to form crystalline secondary cave deposits known as speleothems. The urease family is a group of enzymes involved in MICP that catalyze the breakdown of urea, which is a source of energy, into ammonia and carbonate. Carbonate anions are effluxed to the extracellular surface of the bacterium where it then binds to environmental calcium to form calcium carbonate which then continues to grow in crystal form. Here, we studied bacterial communities from speleothems collected from the Iron Curtain Cave (ICC) in Chilliwack, B.C., Canada, to characterize these organisms and determine whether urease-positive (U+) bacteria were present in the cave and their potential impact on speleothem formation. The ICC is a carbonate cave located on the northside of Chipmunk Ridge, presenting a unique environment with high iron content sediment and limestone structures throughout. With six pools of water throughout the cave, the environment is highly humid, with temperatures ranging between 4 and 12°C depending on the time of year. Ninety-nine bacterial strains were isolated from popcorn (PCS) and soda straw (SSS) speleothems. These isolates were screened for urease enzymatic activity, with 11 candidates found to be urease-positive. After incubation, species-specific crystal morphologies were observed. Popcorn speleothem provided more bacterial diversity overall when compared to soda straw speleothem when examined under a culture-based method. Nearly twice as many U+ isolates were isolated from popcorn speleothems compared to soda straw speleothems. The U+ candidates were identified to the genus level by 16S rRNA analysis, and two isolates underwent whole-genome sequencing. Two novel species were identified as Sphingobacterium sp. PCS056 and Pseudarthrobacter sp. SSS035. Both isolates demonstrated the most crystal production as well as the most morphologically dissimilar crystal shapes in broth culture and were found to produce crystals as previously observed in both agar and broth media. The results from this study are consistent with the involvement of urease-positive bacteria isolated from the ICC in the formation of cave speleothems. 16S rRNA sequencing revealed a diverse set of microbes inhabiting the speleothems that have urease activity. Whole-genome sequencing of the two chosen isolates confirmed the presence of urease pathways, while revealing differences in urease pathway structure and number. This research contributes to understanding microbial-associated cave formation and degradation, with applications to cave conservation, microbiota composition, and their role in shaping the cave environment. |
| first_indexed | 2024-04-13T15:07:46Z |
| format | Article |
| id | doaj.art-69981b7e2eaf40dbafb4fe5163a368b7 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-13T15:07:46Z |
| publishDate | 2022-07-01 |
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| series | Frontiers in Microbiology |
| spelling | doaj.art-69981b7e2eaf40dbafb4fe5163a368b72022-12-22T02:42:06ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-07-011310.3389/fmicb.2022.933388933388Biomineralization in Cave Bacteria—Popcorn and Soda Straw Crystal Formations, Morphologies, and Potential Metabolic PathwaysKeegan Koning0Richenda McFarlane1Jessica T. Gosse2Sara Lawrence3Lynnea Carr4Derrick Horne5Nancy Van Wagoner6Christopher N. Boddy7Naowarat Cheeptham8Department of Biology, Faculty of Science, Thompson Rivers University, Kamloops, BC, CanadaDepartment of Chemistry and Biomolecular Sciences, University of Ottawa, Ottawa, ON, CanadaDepartment of Chemistry and Biomolecular Sciences, University of Ottawa, Ottawa, ON, CanadaDepartment of Biology, Faculty of Science, Thompson Rivers University, Kamloops, BC, CanadaDepartment of Biology, Faculty of Science, Thompson Rivers University, Kamloops, BC, CanadaThe University of British Columbia Bioimaging Facility, Biological Sciences Building, Vancouver, BC, CanadaDepartment of Physical Sciences, Faculty of Science, Thompson Rivers University, Kamloops, BC, CanadaDepartment of Chemistry and Biomolecular Sciences, University of Ottawa, Ottawa, ON, CanadaDepartment of Biology, Faculty of Science, Thompson Rivers University, Kamloops, BC, CanadaCaves are extreme, often oligotrophic, environments that house diverse groups of microorganisms. Many of these microbes can perform microbiologically induced carbonate precipitation (MICP) to form crystalline secondary cave deposits known as speleothems. The urease family is a group of enzymes involved in MICP that catalyze the breakdown of urea, which is a source of energy, into ammonia and carbonate. Carbonate anions are effluxed to the extracellular surface of the bacterium where it then binds to environmental calcium to form calcium carbonate which then continues to grow in crystal form. Here, we studied bacterial communities from speleothems collected from the Iron Curtain Cave (ICC) in Chilliwack, B.C., Canada, to characterize these organisms and determine whether urease-positive (U+) bacteria were present in the cave and their potential impact on speleothem formation. The ICC is a carbonate cave located on the northside of Chipmunk Ridge, presenting a unique environment with high iron content sediment and limestone structures throughout. With six pools of water throughout the cave, the environment is highly humid, with temperatures ranging between 4 and 12°C depending on the time of year. Ninety-nine bacterial strains were isolated from popcorn (PCS) and soda straw (SSS) speleothems. These isolates were screened for urease enzymatic activity, with 11 candidates found to be urease-positive. After incubation, species-specific crystal morphologies were observed. Popcorn speleothem provided more bacterial diversity overall when compared to soda straw speleothem when examined under a culture-based method. Nearly twice as many U+ isolates were isolated from popcorn speleothems compared to soda straw speleothems. The U+ candidates were identified to the genus level by 16S rRNA analysis, and two isolates underwent whole-genome sequencing. Two novel species were identified as Sphingobacterium sp. PCS056 and Pseudarthrobacter sp. SSS035. Both isolates demonstrated the most crystal production as well as the most morphologically dissimilar crystal shapes in broth culture and were found to produce crystals as previously observed in both agar and broth media. The results from this study are consistent with the involvement of urease-positive bacteria isolated from the ICC in the formation of cave speleothems. 16S rRNA sequencing revealed a diverse set of microbes inhabiting the speleothems that have urease activity. Whole-genome sequencing of the two chosen isolates confirmed the presence of urease pathways, while revealing differences in urease pathway structure and number. This research contributes to understanding microbial-associated cave formation and degradation, with applications to cave conservation, microbiota composition, and their role in shaping the cave environment.https://www.frontiersin.org/articles/10.3389/fmicb.2022.933388/fullcave microorganismscave microbiologygeomicrobiologyMICPureasebiomineralization |
| spellingShingle | Keegan Koning Richenda McFarlane Jessica T. Gosse Sara Lawrence Lynnea Carr Derrick Horne Nancy Van Wagoner Christopher N. Boddy Naowarat Cheeptham Biomineralization in Cave Bacteria—Popcorn and Soda Straw Crystal Formations, Morphologies, and Potential Metabolic Pathways Frontiers in Microbiology cave microorganisms cave microbiology geomicrobiology MICP urease biomineralization |
| title | Biomineralization in Cave Bacteria—Popcorn and Soda Straw Crystal Formations, Morphologies, and Potential Metabolic Pathways |
| title_full | Biomineralization in Cave Bacteria—Popcorn and Soda Straw Crystal Formations, Morphologies, and Potential Metabolic Pathways |
| title_fullStr | Biomineralization in Cave Bacteria—Popcorn and Soda Straw Crystal Formations, Morphologies, and Potential Metabolic Pathways |
| title_full_unstemmed | Biomineralization in Cave Bacteria—Popcorn and Soda Straw Crystal Formations, Morphologies, and Potential Metabolic Pathways |
| title_short | Biomineralization in Cave Bacteria—Popcorn and Soda Straw Crystal Formations, Morphologies, and Potential Metabolic Pathways |
| title_sort | biomineralization in cave bacteria popcorn and soda straw crystal formations morphologies and potential metabolic pathways |
| topic | cave microorganisms cave microbiology geomicrobiology MICP urease biomineralization |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.933388/full |
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