Biogeochemical implications of the ubiquitous colonization of marine habitats and redox gradients by Marinobacter species

Handley, Kim M.; Lloyd, Jonathan R.

doi:10.3389/fmicb.2013.00136

Cited by 126Microbial Community Ecology and PhysiologyMicrobial Fuel Cells and BioremediationGeochemistry and Elemental Analysis

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Biogeochemical implications of the ubiquitous colonization of marine habitats and redox gradients by Marinobacter species

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Handley, Kim M., Lloyd, Jonathan R.·2013·Frontiers in Microbiology

DOI 10.3389/fmicb.2013.00136PMC PMC3660661

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Abstract

The Marinobacter genus comprises widespread marine bacteria, found in localities as diverse as the deep ocean, coastal seawater and sediment, hydrothermal settings, oceanic basalt, sea-ice, sand, solar salterns, and oil fields. Terrestrial sources include saline soil and wine-barrel-decalcification wastewater. The genus was designated in 1992 for the Gram-negative, hydrocarbon-degrading bacterium Marinobacter hydrocarbonoclasticus. Since then, a further 31 type strains have been designated. Nonetheless, the metabolic range of many Marinobacter species remains largely unexplored. Most species have been classified as aerobic heterotrophs, and assessed for limited anaerobic pathways (fermentation or nitrate reduction), whereas studies of low-temperature hydrothermal sediments, basalt at oceanic spreading centers, and phytoplankton have identified species that possess a respiratory repertoire with significant biogeochemical implications. Notable physiological traits include nitrate-dependent Fe(II)-oxidation, arsenic and fumarate redox cycling, and Mn(II) oxidation. There is also evidence for Fe(III) reduction, and metal(loid) detoxification. Considering the ubiquity and metabolic capabilities of the genus, Marinobacter species may perform an important and underestimated role in the biogeochemical cycling of organics and metals in varied marine habitats, and spanning aerobic-to-anoxic redox gradients.

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Xu, X.-W., Wu, Y., Wang, C.-S., Yang, J., Oren, A., & Wu, M. (2008) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.65390-0 · Cited by 44
Psychrophiles and Psychrotrophs
Morita, R. Y. (2001) · Encyclopedia of Life Sciences · doi:10.1038/npg.els.0000402 · Cited by 42
Genome Sequence of Deep-Sea Manganese-Oxidizing Bacterium Marinobacter manganoxydans MnI7-9
Wang, H., Li, H., Shao, Z., Liao, S., Johnstone, L. M., Rensing, C., & Wang, G. (2012) · Journal of Bacteriology · doi:10.1128/jb.06551-11 · Cited by 42
The geochemistry of metalliferous sediments and waters associated with shallow submarine hydrothermal activity (Santorini, Aegean Sea)
Smith, P. A., & Cronan, D. S. (1983) · Chemical Geology · doi:10.1016/0009-2541(83)90017-7 · Cited by 41
A Cytochrome cd1-type Nitrite Reductase Isolated from the Marine Denitrifier Pseudomonas nautica 617: Purification and Characterization
Besson, S., Carneiro, C., Moura, J. J. G., Moura, I., & Fauque, G. D. (1995) · Anaerobe · doi:10.1006/anae.1995.1021 · Cited by 37
Production of a Polyunsaturated Isoprenoid Wax Ester during Aerobic Metabolism of Squalene by Marinobacter squalenivorans sp. nov
Rontani, J., Mouzdahir, A., Michotey, V. D., Caumette, P., & Bonin, P. (2003) · Applied and Environmental Microbiology · doi:10.1128/aem.69.7.4167-4176.2003 · Cited by 35
Effects of nitrate treatment on a mixed species, oil field microbial biofilm
Dunsmore, B. C., Youldon, J., Thrasher, D. R., & Vance, I. (2006) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/s10295-006-0095-2 · Cited by 32
Biochemical and spectroscopic characterization of the membrane-bound nitrate reductase from Marinobacter hydrocarbonoclasticus 617
Correia, C., Besson, S., Brondino, C. D., González, P. J., Fauque, G. D., Lampreia, J., Moura, I., & Moura, J. J. G. (2008) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-008-0416-1 · Cited by 30
Marinobacter antarcticus sp. nov., a halotolerant bacterium isolated from Antarctic intertidal sandy sediment
Liu, C., Chen, C., Zhang, X., Yu, Y., Liu, A., Li, G., Chen, X., Chen, B., Zhou, B., & Zhang, Y. (2011) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.035774-0 · Cited by 29
Marinobacter xestospongiae sp. nov., isolated from the marine sponge Xestospongia testudinaria collected from the Red Sea
Lee, O. O., Lai, P. Y., Wu, H., Zhou, X., Miao, L., Wang, H., & Qian, P. (2011) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.028811-0 · Cited by 29
Role of microbial populations in the release of reduced iron to the water column from marine aggregates
Balzano, S., Statham, P. J., Pancost, R. D., & Lloyd, J. R. (2009) · Aquatic Microbial Ecology · doi:10.3354/ame01278 · Cited by 28
Marinobacter salicampi sp. nov., isolated from a marine solar saltern in Korea
Yoon, J., Lee, M., Kang, S.-J., & Oh, T.-K. (2007) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.65197-0 · Cited by 28
Marinobacter mobilis sp. nov. and Marinobacter zhejiangensis sp. nov., halophilic bacteria isolated from the East China Sea
Huo, Y.-Y., Wang, C.-S., Yang, J., Wu, M., & Xu, X. (2008) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.2008/000786-0 · Cited by 26
Marinobacter szutsaonensis sp. nov., isolated from a solar saltern
Wang, C., Ng, C.-C., Tzeng, W.-S., & Shyu, Y. ‐. (2009) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.008896-0 · Cited by 25
Validation of publication of new names and new combinations previously effectively published outside the IJSEM
(2003) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.03001-0 · Cited by 23
Marinobacter goseongensis sp. nov., from seawater
Roh, S. W., Quan, Z., Nam, Y., Chang, H.-W., Kim, K., Rhee, S.-K., Oh, H., Jeon, C. O., Yoon, J., & Bae, J. (2008) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.65522-0 · Cited by 22
Marinobacter lacisalsi sp. nov., a moderately halophilic bacterium isolated from the saline-wetland wildfowl reserve Fuente de Piedra in southern Spain
Aguilera, J., Jiménez-Pranteda, M. L., Kharroub, K., González-Paredes, A., Durbán-Fornieles, J. J., Russell, N. J., Alberto Ramos-cormenzana, A., & Monteoliva‐Sánchez, M. (2009) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.007518-0 · Cited by 19
Microbial and hydrothermal aspects of ferric oxyhydroxides and ferrosic hydroxides: the example of Franklin Seamount, Western Woodlark Basin, Papua New Guinea
Boyd, T., & Scott, S. D. (2001) · Geochemical Transactions · doi:10.1039/b105277m · Cited by 17
Microbial diversity analysis of former salterns in southern Taiwan by 16S rRNA‐based methods
Wang, C., Ng, C., Chen, T., Wu, S., & Shyu, Y. (2007) · Journal of Basic Microbiology · doi:10.1002/jobm.200700250 · Cited by 16
Marinobacter zhanjiangensis sp. nov., a marine bacterium isolated from sea water of a tidal flat of the South China Sea
Da-chun, Z., Chen, Y., Zhang, Y., Tang, S., Wu, X., Tan, Z.-C., Li, W., & Cui, X. (2009) · Antonie van Leeuwenhoek · doi:10.1007/s10482-009-9344-5 · Cited by 15
Marinobacter oulmenensis sp. nov., a moderately halophilic bacterium isolated from brine of a salt concentrator
Kharroub, K., Aguilera, J., Jiménez-Pranteda, M. L., González-Paredes, A., Alberto Ramos-cormenzana, A., & Monteoliva‐Sánchez, M. (2010) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.027284-0 · Cited by 15
High incidence of halotolerant bacteria in Pacific hydrothermal-vent and pelagic environments
Kaye, J. Z. (2000) · FEMS Microbiology Ecology · doi:10.1016/s0168-6496(00)00035-0 · Cited by 15
Marinobacter daqiaonensis sp. nov., a moderate halophile isolated from a Yellow Sea salt pond
Qu, L., Zhu, F., Zhang, J., Gao, C., & Sun, X. (2011) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.028993-0 · Cited by 12
Biogeochemical controls on microbial diversity in seafloor sulphidic sediments
Müller, M., Handley, K. M., Lloyd, J. R., Pancost, R. D., & Mills, R. A. (2010) · Geobiology · doi:10.1111/j.1472-4669.2010.00242.x · Cited by 7
Genome Sequence of Hydrothermal Arsenic-Respiring Bacterium Marinobacter santoriniensis NKSG1 T
Handley, K. M., Upton, M., Beatson, S. A., Héry, M., & Lloyd, J. R. (2013) · Genome Announcements · doi:10.1128/genomea.00231-13 · Cited by 5
Marinobacter santoriniensis sp. nov., an arsenate-respiring and arsenite-oxidizing bacterium isolated from hydrothermal sediment
Handley, K. M., Héry, M., & Lloyd, J. R. (2009) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/00207713-59-7-1850-b · Cited by 4
Sulfate reduction and possible aerobic metabolism of the sulfate-reducing bacterium Desulfovibrio oxyclinae in a chemostat coculture with Marinobacter sp. strain MB under exposure to increasing oxygen concentrations
Cohen, Y., Sigalevich, P., Teske, A., et al. (2022) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/v33s-4784 · Cited by 2
Microbial diversity analysis of former salterns in southern Taiwan by 16S rRNA-based methods
Wang, C., & Shyu, Y. (2008) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2008.07.1426 · Cited by 1
Structure and composition of the Aleutian island arc and implications for continental crustal growth
Steven Holbrook, W., Lizarralde, D., McGeary, S., Bangs, N., & Diebold, J. (1999) · Geology · doi:10.1130/0091-7613(1999)027

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Unexplored microbial diversity from 2,500 food metagenomes and links with the human microbiome.
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High Growth Potential of Long-Term Starved Deep Ocean Opportunistic Heterotrophic Bacteria
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Review
H, K. M., Lloyd, J. R., Purificacion Lopez-garcia Centre, H, K. M., & Chemistry, S. (2016)
Metabolic versatility of Marinobacter and its biotechnological potential
Cheng, L., Zhu, P., Ke, H., Hou, S., Luo, Q., & Lü, X. (2025) · Biotechnology Advances · doi:10.1016/j.biotechadv.2025.108650 · Cited by 6
Substrates specialization in lipid compounds and hydrocarbons of Marinobacter genus
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Genome Sequence of Hydrothermal Arsenic-Respiring Bacterium
Nksgt, M. S., H, K. M., Upton, A. M., Beatson, S. A., Héry, C. M., Lloyda, A. J. R., & Lloyd, O. J. R. (2013)
Genome Sequence of Hydrothermal Arsenic-Respiring Bacterium Marinobacter santoriniensis NKSG1 T
Handley, K. M., Upton, M., Beatson, S. A., Héry, M., & Lloyd, J. R. (2013) · Genome Announcements · doi:10.1128/genomea.00231-13 · Cited by 5

Authors: Handley, K. M., & Lloyd, J. R.
Affiliations: Argonne National Laboratory (US)
University of Manchester (GB)
Corresponding author: Handley, Kim M.
ORCID: Handley, Kim M.
Lloyd, Jonathan R.
Venue: Frontiers in Microbiology
Publisher: Frontiers Media SA
Published: 2013
Volume: 4
Pages: 136-136
ISSN: 1664-302X (ISSN-L)
DOI: 10.3389/fmicb.2013.00136
PMC: PMC3660661
OpenAlex: W2099533595
Cited by: 126
References: 109
Citations by year: 2026: 18 · 2025: 14 · 2024: 17 · 2023: 7 · 2022: 12 · 2021: 14 · 2020: 15 · 2019: 11 · 2018: 5 · 2017: 6 · 2016: 2 · 2015: 5
FWCI: 2.06
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Frontiers in Microbiology (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Research Explorer (The University of Manchester) (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
ResearchSpace (University of Auckland) (submittedVersion, cc-by)
Funders: European Commission
Topics: Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Physical Sciences › Environmental Science › Environmental Engineering › Microbial Fuel Cells and Bioremediation
Physical Sciences › Earth and Planetary Sciences › Geochemistry and Petrology › Geochemistry and Elemental Analysis
Keywords: Marinobacter, marine bacteria, biogeochemical cycles, redox gradients, fumarate respiration, Mn(II) oxidation, Fe(III) reduction, hydrocarbon-degrading bacteria, hydrothermal sediments, oceanic basalts, marine sediment, anaerobic metabolism

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Biogeochemical implications of the ubiquitous colonization of marine habitats and redox gradients by Marinobacter species

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