Niche differentiation among sulfur-oxidizing bacterial populations in cave waters

Jennifer L. Macalady; Sharmishtha Dattagupta; Irene Schaperdoth; Daniel S. Jones; Greg K. Druschel; Danielle Eastman

doi:10.1038/ismej.2008.25

Niche differentiation among sulfur-oxidizing bacterial populations in cave waters

Jennifer L. Macalady, Sharmishtha Dattagupta, Irene Schaperdoth, Daniel S. Jones, Greg K. Druschel, Danielle Eastman

Research output: Contribution to journal › Article › peer-review

150 Scopus citations

Abstract

The sulfidic Frasassi cave system affords a unique opportunity to investigate niche relationships among sulfur-oxidizing bacteria, including epsilonproteobacterial clades with no cultivated representatives. Oxygen and sulfide concentrations in the cave waters range over more than two orders of magnitude as a result of seasonally and spatially variable dilution of the sulfidic groundwater. A full-cycle rRNA approach was used to quantify dominant populations in biofilms collected in both diluted and undiluted zones. Sulfide concentration profiles within biofilms were obtained in situ using microelectrode voltammetry. Populations in rock-attached streamers depended on the sulfide/oxygen supply ratio of bulk water (r0.97; P0.0001). Filamentous epsilonproteobacteria dominated at high sulfide to oxygen ratios (150), whereas Thiothrix dominated at low ratios (75). In contrast, Beggiatoa was the dominant group in biofilms at the sediment-water interface regardless of sulfide and oxygen concentrations or supply ratio. Our results highlight the versatility and ecological success of Beggiatoa in diffusion-controlled niches, and demonstrate that high sulfide/oxygen ratios in turbulent water are important for the growth of filamentous epsilonproteobacteria.

Original language	English (US)
Pages (from-to)	590-601
Number of pages	12
Journal	ISME Journal
Volume	2
Issue number	6
DOIs	https://doi.org/10.1038/ismej.2008.25
State	Published - Jun 2008

All Science Journal Classification (ASJC) codes

Microbiology
Ecology, Evolution, Behavior and Systematics

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10.1038/ismej.2008.25

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@article{5835a5a78e93424da37f2c3ca78c66f8,

title = "Niche differentiation among sulfur-oxidizing bacterial populations in cave waters",

abstract = "The sulfidic Frasassi cave system affords a unique opportunity to investigate niche relationships among sulfur-oxidizing bacteria, including epsilonproteobacterial clades with no cultivated representatives. Oxygen and sulfide concentrations in the cave waters range over more than two orders of magnitude as a result of seasonally and spatially variable dilution of the sulfidic groundwater. A full-cycle rRNA approach was used to quantify dominant populations in biofilms collected in both diluted and undiluted zones. Sulfide concentration profiles within biofilms were obtained in situ using microelectrode voltammetry. Populations in rock-attached streamers depended on the sulfide/oxygen supply ratio of bulk water (r0.97; P0.0001). Filamentous epsilonproteobacteria dominated at high sulfide to oxygen ratios (150), whereas Thiothrix dominated at low ratios (75). In contrast, Beggiatoa was the dominant group in biofilms at the sediment-water interface regardless of sulfide and oxygen concentrations or supply ratio. Our results highlight the versatility and ecological success of Beggiatoa in diffusion-controlled niches, and demonstrate that high sulfide/oxygen ratios in turbulent water are important for the growth of filamentous epsilonproteobacteria.",

author = "Macalady, {Jennifer L.} and Sharmishtha Dattagupta and Irene Schaperdoth and Jones, {Daniel S.} and Druschel, {Greg K.} and Danielle Eastman",

note = "Funding Information: This paper was improved by the comments of three anonymous reviewers. We thank A Montanari for logistical support and the use of facilities and laboratory space at the Osservatorio Geologico di Coldigioco (Italy) and S Mariani, S Galdenzi and S Cerioni for expert advice and field assitance. We also thank P D{\textquoteright}Eugenio, M Mainiero, S Recanatini, R Hegemann, H Albrecht, K Freeman and R Grymes for assistance in the field. We thank B Thomas and J Moore for water analyses, and L Albertson and T Stoffer for laboratory assistance. E Fleming provided valuable comments on the paper. DE contributed to this research as an undergraduate student and was supported in 2006 by a Barrett Foundation scholarship. This work was supported by grants to JLM from the Biogeosciences Program of the National Science Foundation (EAR 0311854 and EAR 0527046) and NASA NAI (NNA04CC06A). GKD acknowledges support from the American Chemical Society Petroleum Research Fund (43356-GB2) and NSF-EPS-CoR-VT (EPS 0236976).",

year = "2008",

month = jun,

doi = "10.1038/ismej.2008.25",

language = "English (US)",

volume = "2",

pages = "590--601",

journal = "ISME Journal",

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T1 - Niche differentiation among sulfur-oxidizing bacterial populations in cave waters

AU - Macalady, Jennifer L.

AU - Dattagupta, Sharmishtha

AU - Schaperdoth, Irene

AU - Jones, Daniel S.

AU - Druschel, Greg K.

AU - Eastman, Danielle

N1 - Funding Information: This paper was improved by the comments of three anonymous reviewers. We thank A Montanari for logistical support and the use of facilities and laboratory space at the Osservatorio Geologico di Coldigioco (Italy) and S Mariani, S Galdenzi and S Cerioni for expert advice and field assitance. We also thank P D’Eugenio, M Mainiero, S Recanatini, R Hegemann, H Albrecht, K Freeman and R Grymes for assistance in the field. We thank B Thomas and J Moore for water analyses, and L Albertson and T Stoffer for laboratory assistance. E Fleming provided valuable comments on the paper. DE contributed to this research as an undergraduate student and was supported in 2006 by a Barrett Foundation scholarship. This work was supported by grants to JLM from the Biogeosciences Program of the National Science Foundation (EAR 0311854 and EAR 0527046) and NASA NAI (NNA04CC06A). GKD acknowledges support from the American Chemical Society Petroleum Research Fund (43356-GB2) and NSF-EPS-CoR-VT (EPS 0236976).

PY - 2008/6

Y1 - 2008/6

N2 - The sulfidic Frasassi cave system affords a unique opportunity to investigate niche relationships among sulfur-oxidizing bacteria, including epsilonproteobacterial clades with no cultivated representatives. Oxygen and sulfide concentrations in the cave waters range over more than two orders of magnitude as a result of seasonally and spatially variable dilution of the sulfidic groundwater. A full-cycle rRNA approach was used to quantify dominant populations in biofilms collected in both diluted and undiluted zones. Sulfide concentration profiles within biofilms were obtained in situ using microelectrode voltammetry. Populations in rock-attached streamers depended on the sulfide/oxygen supply ratio of bulk water (r0.97; P0.0001). Filamentous epsilonproteobacteria dominated at high sulfide to oxygen ratios (150), whereas Thiothrix dominated at low ratios (75). In contrast, Beggiatoa was the dominant group in biofilms at the sediment-water interface regardless of sulfide and oxygen concentrations or supply ratio. Our results highlight the versatility and ecological success of Beggiatoa in diffusion-controlled niches, and demonstrate that high sulfide/oxygen ratios in turbulent water are important for the growth of filamentous epsilonproteobacteria.

AB - The sulfidic Frasassi cave system affords a unique opportunity to investigate niche relationships among sulfur-oxidizing bacteria, including epsilonproteobacterial clades with no cultivated representatives. Oxygen and sulfide concentrations in the cave waters range over more than two orders of magnitude as a result of seasonally and spatially variable dilution of the sulfidic groundwater. A full-cycle rRNA approach was used to quantify dominant populations in biofilms collected in both diluted and undiluted zones. Sulfide concentration profiles within biofilms were obtained in situ using microelectrode voltammetry. Populations in rock-attached streamers depended on the sulfide/oxygen supply ratio of bulk water (r0.97; P0.0001). Filamentous epsilonproteobacteria dominated at high sulfide to oxygen ratios (150), whereas Thiothrix dominated at low ratios (75). In contrast, Beggiatoa was the dominant group in biofilms at the sediment-water interface regardless of sulfide and oxygen concentrations or supply ratio. Our results highlight the versatility and ecological success of Beggiatoa in diffusion-controlled niches, and demonstrate that high sulfide/oxygen ratios in turbulent water are important for the growth of filamentous epsilonproteobacteria.

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JF - ISME Journal

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Niche differentiation among sulfur-oxidizing bacterial populations in cave waters

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