Articles | Volume 18, issue 4
https://doi.org/10.5194/bg-18-1463-2021
© Author(s) 2021. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
https://doi.org/10.5194/bg-18-1463-2021
© Author(s) 2021. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Research article
| 
01 Mar 2021
Research article |
| 01 Mar 2021
| 01 Mar 2021
Novel hydrocarbon-utilizing soil mycobacteria synthesize unique mycocerosic acids at a Sicilian everlasting fire
Nadine T. Smit
CORRESPONDING AUTHOR
NIOZ Royal Netherlands Institute for Sea Research, Department of
Marine Microbiology and Biogeochemistry, P.O. Box 59, 1790 AB Den Burg, Texel, the Netherlands
Laura Villanueva
NIOZ Royal Netherlands Institute for Sea Research, Department of
Marine Microbiology and Biogeochemistry, P.O. Box 59, 1790 AB Den Burg, Texel, the Netherlands
Department of Earth Sciences, Faculty of Geosciences, Utrecht
University, P.O. Box 80.121, 3508 TA Utrecht, the Netherlands
Darci Rush
NIOZ Royal Netherlands Institute for Sea Research, Department of
Marine Microbiology and Biogeochemistry, P.O. Box 59, 1790 AB Den Burg, Texel, the Netherlands
Fausto Grassa
Istituto Nazionale di Geofisica e Vulcanologia, Sezione di Palermo,
Via Ugo La Malfa, 153, 90146, Palermo, Italy
Caitlyn R. Witkowski
NIOZ Royal Netherlands Institute for Sea Research, Department of
Marine Microbiology and Biogeochemistry, P.O. Box 59, 1790 AB Den Burg, Texel, the Netherlands
Mira Holzheimer
Stratingh Institute for Chemistry, University of Groningen, 9747 AG
Groningen, the Netherlands
Adriaan J. Minnaard
Stratingh Institute for Chemistry, University of Groningen, 9747 AG
Groningen, the Netherlands
Jaap S. Sinninghe Damsté
NIOZ Royal Netherlands Institute for Sea Research, Department of
Marine Microbiology and Biogeochemistry, P.O. Box 59, 1790 AB Den Burg, Texel, the Netherlands
Department of Earth Sciences, Faculty of Geosciences, Utrecht
University, P.O. Box 80.121, 3508 TA Utrecht, the Netherlands
Stefan Schouten
NIOZ Royal Netherlands Institute for Sea Research, Department of
Marine Microbiology and Biogeochemistry, P.O. Box 59, 1790 AB Den Burg, Texel, the Netherlands
Department of Earth Sciences, Faculty of Geosciences, Utrecht
University, P.O. Box 80.121, 3508 TA Utrecht, the Netherlands
Related authors
No articles found.
Anna Cutmore, Nicole Bale, Rick Hennekam, Bingjie Yang, Darci Rush, Gert-Jan Reichart, Ellen C. Hopmans, and Stefan Schouten
Clim. Past, 21, 957–971, https://doi.org/10.5194/cp-21-957-2025, https://doi.org/10.5194/cp-21-957-2025, 2025
Short summary
Short summary
As human activities lower marine oxygen levels, understanding the impact on the marine nitrogen cycle is vital. The Black Sea, which became oxygen-deprived 9600 years ago, offers key insights. By studying organic compounds linked to nitrogen cycle processes, we found that, 7200 years ago, the Black Sea's nitrogen cycle significantly altered due to severe deoxygenation. This suggests that continued marine oxygen decline could similarly alter the marine nitrogen cycle, affecting vital ecosystems.
Anna Cutmore, Nora Richter, Nicole Bale, Stefan Schouten, and Darci Rush
EGUsphere, https://doi.org/10.5194/egusphere-2025-1796, https://doi.org/10.5194/egusphere-2025-1796, 2025
Short summary
Short summary
This study uses bacterial compounds, bacteriohopanepolyols (BHPs), preserved in Black Sea sediments to trace major environmental changes over the past 20,000 years. As the basin shifted from a freshwater lake to a permanently oxygen-poor marine environment, we observe clear changes in bacterial communities and environmental conditions. These findings offer new insight into how microbes responded to significant hydrological changes during the last deglaciation and Holocene.
Peter Kraal, Kristin A. Ungerhofer, Darci Rush, and Gert-Jan Reichart
EGUsphere, https://doi.org/10.5194/egusphere-2025-1870, https://doi.org/10.5194/egusphere-2025-1870, 2025
This preprint is open for discussion and under review for Biogeosciences (BG).
Short summary
Short summary
Element cycles in oxygen-depleted areas such as upwelling areas inform future deoxygenation scenarios. The Benguela upwelling system shows strong decoupling of nitrogen and phosphorus cycling due to seasonal shelf anoxia. Anaerobic processes result in pelagic nitrogen loss as N2. At the same time, sediments are rich in fish-derived and bacterial phosphorus, with high fluxes of excess phosphate, altering deep-water nitrogen:phosphorus ratios. Such alterations can affect ocean functioning.
Szabina Karancz, Lennart J. de Nooijer, Bas van der Wagt, Marcel T. J. van der Meer, Sambuddha Misra, Rick Hennekam, Zeynep Erdem, Julie Lattaud, Negar Haghipour, Stefan Schouten, and Gert-Jan Reichart
Clim. Past, 21, 679–704, https://doi.org/10.5194/cp-21-679-2025, https://doi.org/10.5194/cp-21-679-2025, 2025
Short summary
Short summary
Changes in upwelling intensity of the Benguela upwelling region during the last glacial motivated us to investigate the local CO2 history during the last glacial-to-interglacial transition. Using various geochemical tracers on archives from both subsurface and surface waters reveals enhanced storage of carbon at depth during the Last Glacial Maximum. An efficient biological pump likely prevented outgassing of CO2 from intermediate depth to the atmosphere.
Devika Varma, Laura Villanueva, Nicole J. Bale, Pierre Offre, Gert-Jan Reichart, and Stefan Schouten
Biogeosciences, 21, 4875–4888, https://doi.org/10.5194/bg-21-4875-2024, https://doi.org/10.5194/bg-21-4875-2024, 2024
Short summary
Short summary
Archaeal hydroxylated tetraether lipids are increasingly used as temperature indicators in marine settings, but the factors influencing their distribution are still unclear. Analyzing membrane lipids of two thaumarchaeotal strains showed that the growth phase of the cultures does not affect the lipid distribution, but growth temperature profoundly affects the degree of cyclization of these lipids. Also, the abundance of these lipids is species-specific and is not influenced by temperature.
Guangnan Wu, Klaas G. J. Nierop, Bingjie Yang, Stefan Schouten, Gert-Jan Reichart, and Peter Kraal
EGUsphere, https://doi.org/10.5194/egusphere-2024-3192, https://doi.org/10.5194/egusphere-2024-3192, 2024
Short summary
Short summary
Estuaries store and process large amounts of carbon, making them vital to the global carbon cycle. In the Port of Rotterdam, we studied the source of organic matter (OM) in sediments and how it influences OM breakdown. We found that marine OM degrades faster than land OM, and human activities like dredging can accelerate this by exposing sediments to oxygen. Our findings highlight the impact of human activities on carbon storage in estuaries, which is key for managing estuarine carbon dynamics.
Allix J. Baxter, Francien Peterse, Dirk Verschuren, Aihemaiti Maitituerdi, Nicolas Waldmann, and Jaap S. Sinninghe Damsté
Biogeosciences, 21, 2877–2908, https://doi.org/10.5194/bg-21-2877-2024, https://doi.org/10.5194/bg-21-2877-2024, 2024
Short summary
Short summary
This study investigates the impact of long-term lake-system evolution on the climate signal recorded by glycerol dialkyl glycerol tetraethers (GDGTs), a popular biomarker in paleoclimate research. It compares downcore changes in GDGTs in the 250 000 year sediment sequence of Lake Chala (Kenya/Tanzania) to independent data for lake mixing and water-column chemistry. These factors influence the GDGT proxies in the earliest depositional phases (before ~180 ka), confounding the climate signal.
Zoë Rebecca van Kemenade, Zeynep Erdem, Ellen Christine Hopmans, Jaap Smede Sinninghe Damsté, and Darci Rush
Biogeosciences, 21, 1517–1532, https://doi.org/10.5194/bg-21-1517-2024, https://doi.org/10.5194/bg-21-1517-2024, 2024
Short summary
Short summary
The California Current system (CCS) hosts the eastern subtropical North Pacific oxygen minimum zone (ESTNP OMZ). This study shows anaerobic ammonium oxidizing (anammox) bacteria cause a loss of bioavailable nitrogen (N) in the ESTNP OMZ throughout the late Quaternary. Anammox occurred during both glacial and interglacial periods and was driven by the supply of organic matter and changes in ocean currents. These findings may have important consequences for biogeochemical models of the CCS.
Vera Dorothee Meyer, Jürgen Pätzold, Gesine Mollenhauer, Isla S. Castañeda, Stefan Schouten, and Enno Schefuß
Clim. Past, 20, 523–546, https://doi.org/10.5194/cp-20-523-2024, https://doi.org/10.5194/cp-20-523-2024, 2024
Short summary
Short summary
The climatic factors sustaining vegetation in the Sahara during the African humid period (AHP) are still not fully understood. Using biomarkers in a marine sediment core from the eastern Mediterranean, we infer variations in Mediterranean (winter) and monsoonal (summer) rainfall in the Nile river watershed around the AHP. We find that winter and summer rain enhanced during the AHP, suggesting that Mediterranean moisture supported the monsoon in sustaining the “green Sahara”.
Katrin Hättig, Devika Varma, Stefan Schouten, and Marcel T. J. van der Meer
Clim. Past, 19, 1919–1930, https://doi.org/10.5194/cp-19-1919-2023, https://doi.org/10.5194/cp-19-1919-2023, 2023
Short summary
Short summary
Water isotopes, both hydrogen and oxygen, correlate with the salinity of the sea. Here we reconstruct the surface seawater isotopic composition during the last deglaciation based on the measured hydrogen isotopic composition of alkenones, organic compounds derived from haptophyte algae, and compared it to oxygen isotopes of calcite shells produced in the bottom water. Our results suggest that surface seawater experienced more freshening during the last 20 000 years than the bottom seawater.
Nora Richter, Ellen C. Hopmans, Danica Mitrović, Pedro M. Raposeiro, Vítor Gonçalves, Ana C. Costa, Linda A. Amaral-Zettler, Laura Villanueva, and Darci Rush
Biogeosciences, 20, 2065–2098, https://doi.org/10.5194/bg-20-2065-2023, https://doi.org/10.5194/bg-20-2065-2023, 2023
Short summary
Short summary
Bacteriohopanepolyols (BHPs) are a diverse class of lipids produced by bacteria across a wide range of environments. This study characterizes the diversity of BHPs in lakes and coastal lagoons in the Azores Archipelago, as well as a co-culture enriched for methanotrophs. We highlight the potential of BHPs as taxonomic markers for bacteria associated with certain ecological niches, which can be preserved in sedimentary records.
Caitlyn R. Witkowski, Vittoria Lauretano, Alex Farnsworth, Shufeng Li, Shi-Hu Li, Jan Peter Mayser, B. David A. Naafs, Robert A. Spicer, Tao Su, He Tang, Zhe-Kun Zhou, Paul J. Valdes, and Richard D. Pancost
EGUsphere, https://doi.org/10.5194/egusphere-2023-373, https://doi.org/10.5194/egusphere-2023-373, 2023
Preprint archived
Short summary
Short summary
Untangling the complex tectonic evolution in the Tibetan region can help us understand its impacts on climate, the Asian monsoon system, and the development of major biodiversity hotspots. We show that this “missing link” site between high elevation Tibet and low elevation coastal China had a dynamic environment but no temperature change, meaning its been at its current-day elevation for the past 34 million years.
Kasia K. Śliwińska, Helen K. Coxall, David K. Hutchinson, Diederik Liebrand, Stefan Schouten, and Agatha M. de Boer
Clim. Past, 19, 123–140, https://doi.org/10.5194/cp-19-123-2023, https://doi.org/10.5194/cp-19-123-2023, 2023
Short summary
Short summary
We provide a sea surface temperature record from the Labrador Sea (ODP Site 647) based on organic geochemical proxies across the late Eocene and early Oligocene. Our study reveals heterogenic cooling of the Atlantic. The cooling of the North Atlantic is difficult to reconcile with the active Atlantic Meridional Overturning Circulation (AMOC). We discuss possible explanations like uncertainty in the data, paleogeography and atmospheric CO2 boundary conditions, model weaknesses, and AMOC activity.
Jaap S. Sinninghe Damsté, Lisa A. Warden, Carlo Berg, Klaus Jürgens, and Matthias Moros
Clim. Past, 18, 2271–2288, https://doi.org/10.5194/cp-18-2271-2022, https://doi.org/10.5194/cp-18-2271-2022, 2022
Short summary
Short summary
Reconstruction of past climate conditions is important for understanding current climate change. These reconstructions are derived from proxies, enabling reconstructions of, e.g., past temperature, precipitation, vegetation, and sea surface temperature (SST). Here we investigate a recently developed SST proxy based on membrane lipids of ammonium-oxidizing archaea in the ocean. We show that low salinities substantially affect the proxy calibration by examining Holocene Baltic Sea sediments.
Carolien M. H. van der Weijst, Koen J. van der Laan, Francien Peterse, Gert-Jan Reichart, Francesca Sangiorgi, Stefan Schouten, Tjerk J. T. Veenstra, and Appy Sluijs
Clim. Past, 18, 1947–1962, https://doi.org/10.5194/cp-18-1947-2022, https://doi.org/10.5194/cp-18-1947-2022, 2022
Short summary
Short summary
The TEX86 proxy is often used by paleoceanographers to reconstruct past sea-surface temperatures. However, the origin of the TEX86 signal in marine sediments has been debated since the proxy was first proposed. In our paper, we show that TEX86 carries a mixed sea-surface and subsurface temperature signal and should be calibrated accordingly. Using our 15-million-year record, we subsequently show how a TEX86 subsurface temperature record can be used to inform us on past sea-surface temperatures.
Zoë R. van Kemenade, Laura Villanueva, Ellen C. Hopmans, Peter Kraal, Harry J. Witte, Jaap S. Sinninghe Damsté, and Darci Rush
Biogeosciences, 19, 201–221, https://doi.org/10.5194/bg-19-201-2022, https://doi.org/10.5194/bg-19-201-2022, 2022
Short summary
Short summary
Anaerobic ammonium oxidation (anammox) is an important nitrogen-removal process in the ocean. We assess the distribution of bacteriohopanetetrol-x (BHT-x), used to trace past anammox, along a redox gradient in the water column of the Benguela upwelling system. BHT-x / BHT ratios of >0.18 correspond to the presence of living anammox bacteria and oxygen levels <50 μmol L−1. This allows for a more robust application of BHT-x to trace past marine anammox and deoxygenation in dynamic marine systems.
Alessandro Gattuso, Francesco Italiano, Giorgio Capasso, Antonino D'Alessandro, Fausto Grassa, Antonino Fabio Pisciotta, and Davide Romano
Nat. Hazards Earth Syst. Sci., 21, 3407–3419, https://doi.org/10.5194/nhess-21-3407-2021, https://doi.org/10.5194/nhess-21-3407-2021, 2021
Short summary
Short summary
Santa Barbara and Aragona are affected by mud volcanism with episodic hazardous paroxysm events. Two potentially hazardous paroxysm exposed surfaces of 0.12 and 0.20 km2 were elaborated with DSMs and with historical information on the paroxysms that occurred in the past. This paper, in the end, could be a useful tool for civil protection authorities in order to take appropriate risk mitigation measurements for exposed people and for monitoring activities.
Charlotte L. Spencer-Jones, Erin L. McClymont, Nicole J. Bale, Ellen C. Hopmans, Stefan Schouten, Juliane Müller, E. Povl Abrahamsen, Claire Allen, Torsten Bickert, Claus-Dieter Hillenbrand, Elaine Mawbey, Victoria Peck, Aleksandra Svalova, and James A. Smith
Biogeosciences, 18, 3485–3504, https://doi.org/10.5194/bg-18-3485-2021, https://doi.org/10.5194/bg-18-3485-2021, 2021
Short summary
Short summary
Long-term ocean temperature records are needed to fully understand the impact of West Antarctic Ice Sheet collapse. Glycerol dialkyl glycerol tetraethers (GDGTs) are powerful tools for reconstructing ocean temperature but can be difficult to apply to the Southern Ocean. Our results show active GDGT synthesis in relatively warm depths of the ocean. This research improves the application of GDGT palaeoceanographic proxies in the Southern Ocean.
Cécile L. Blanchet, Rik Tjallingii, Anja M. Schleicher, Stefan Schouten, Martin Frank, and Achim Brauer
Clim. Past, 17, 1025–1050, https://doi.org/10.5194/cp-17-1025-2021, https://doi.org/10.5194/cp-17-1025-2021, 2021
Short summary
Short summary
The Mediterranean Sea turned repeatedly into an oxygen-deprived basin during the geological past, as evidenced by distinct sediment layers called sapropels. We use here records of the last sapropel S1 retrieved in front of the Nile River to explore the relationships between riverine input and seawater oxygenation. We decipher the seasonal cycle of fluvial input and seawater chemistry as well as the decisive influence of primary productivity on deoxygenation at millennial timescales.
Appy Sluijs, Joost Frieling, Gordon N. Inglis, Klaas G. J. Nierop, Francien Peterse, Francesca Sangiorgi, and Stefan Schouten
Clim. Past, 16, 2381–2400, https://doi.org/10.5194/cp-16-2381-2020, https://doi.org/10.5194/cp-16-2381-2020, 2020
Short summary
Short summary
We revisit 15-year-old reconstructions of sea surface temperatures in the Arctic Ocean for the late Paleocene and early Eocene epochs (∼ 57–53 million years ago) based on the distribution of fossil membrane lipids of archaea preserved in Arctic Ocean sediments. We find that improvements in the methods over the past 15 years do not lead to different results. However, data quality is now higher and potential biases better characterized. Results confirm remarkable Arctic warmth during this time.
Loes G. J. van Bree, Francien Peterse, Allix J. Baxter, Wannes De Crop, Sigrid van Grinsven, Laura Villanueva, Dirk Verschuren, and Jaap S. Sinninghe Damsté
Biogeosciences, 17, 5443–5463, https://doi.org/10.5194/bg-17-5443-2020, https://doi.org/10.5194/bg-17-5443-2020, 2020
Short summary
Short summary
Branched glycerol dialkyl glycerol tetraethers (brGDGTs) are used as a paleothermometer based on their temperature dependence in global soils, but aquatic production complicates their use in lakes. BrGDGTs in the water column of Lake Chala, East Africa, respond to oxygen conditions and mixing. Changes in their signal can be linked to bacterial community composition rather than membrane adaptation to changing conditions. Their integrated signal in the sediment reflects mean air temperature.
Cited articles
Abdala Asbun, A., Besseling, M. A., Balzano, S., van Bleijswijk, J. D. L.,
Witte, H. J., Villanueva, L., and Engelmann, J. C.: Cascabel: A Scalable and Versatile Amplicon Sequence Data Analysis Pipeline Delivering Reproducible and Documented Results, Frontiers in Genetics, 11, 1329,
https://doi.org/10.3389/fgene.2020.489357, 2020.
Ahmed, M., Schouten, S., Baas, M., and De Leeuw, J.: Bound lipids in
kerogens from the Monterey Formation, Naples Beach, California, The Monterey
Formation: From Rock to Molecules, Columbia University Press, New York,
189–205, 2001.
Alugupalli, S., Sikka, M. K., Larsson, L., and White, D. C.: Gas
chromatography–mass spectrometry methods for the analysis of mycocerosic
acids present in Mycobacterium tuberculosis, J. Microbiol. Meth., 31, 143–150, 1998.
Andrews, S.: FastQC: a quality control tool for high throughput sequence
data, available at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc (last access: 5 August 2018), 2010.
Bale, N. J., Villanueva, L., Hopmans, E. C., Schouten, S., and Sinninghe Damsté, J. S.: Different seasonality of pelagic and benthic Thaumarchaeota in the North Sea, Biogeosciences, 10, 7195–7206, https://doi.org/10.5194/bg-10-7195-2013, 2013.
Balesdent, J., Mariotti, A., and Guillet, B.: Natural 13C abundance as
a tracer for studies of soil organic matter dynamics, Soil Biol. Biochem., 19, 25–30, 1987.
Bardgett, R. D. and van der Putten, W. H.: Belowground biodiversity and
ecosystem functioning, Nature, 515, 505–511, 2014.
Basilone, L.: Litostratigrafia della Sicilia, Dipartimento di scienze della
terra e del mare, Università degli studi, Arti Grafiche Palermitane s.r.l, Palermo, Italy, ISBN: 978-88-97559-09-2, 2012.
Berndmeyer, C., Thiel, V., Schmale, O., and Blumenberg, M.: Biomarkers for
aerobic methanotrophy in the water column of the stratified Gotland Deep
(Baltic Sea), Org. Geochem., 55, 103–111, 2013.
Besseling, M. A., Hopmans, E. C., Boschman, R. C., Sinninghe Damsté, J. S., and Villanueva, L.: Benthic archaea as potential sources of tetraether membrane lipids in sediments across an oxygen minimum zone, Biogeosciences, 15, 4047–4064, https://doi.org/10.5194/bg-15-4047-2018, 2018.
Birgel, D. and Peckmann, J.: Aerobic methanotrophy at ancient marine
methane seeps: a synthesis, Org. Geochem., 39, 1659–1667, 2008.
Blumenberg, M., Seifert, R., and Michaelis, W.: Aerobic methanotrophy in the
oxic–anoxic transition zone of the Black Sea water column, Org. Geochem., 38, 84–91, 2007.
Bodelier, P. L., Gillisen, M.-J. B., Hordijk, K., Sinninghe Damsté, J.
S., Rijpstra, W. I. C., Geenevasen, J. A., and Dunfield, P. F.: A reanalysis
of phospholipid fatty acids as ecological biomarkers for methanotrophic
bacteria, The ISME journal, 3, 606–617, 2009.
Bouam, A., Armstrong, N., Levasseur, A., and Drancourt, M.: Mycobacterium
terramassiliense, Mycobacterium rhizamassiliense and Mycobacterium
numidiamassiliense sp. nov., three new Mycobacterium simiae complex species
cultured from plant roots, Scientific Reports, 8, 1–13, 2018.
Bowman, J.: The methanotrophs – the families Methylococcaceae and
Methylocystaceae, The Prokaryotes, 5, 266–289, 2006.
Bowman, J. P., Sly, L. I., Nichols, P. D., and Hayward, A.: Revised taxonomy
of the methanotrophs: description of Methylobacter gen. nov., emendation of
Methylococcus, validation of Methylosinus and Methylocystis species, and a
proposal that the family Methylococcaceae includes only the group I
methanotrophs, Int. J. Syst. Evol. Micr., 43, 735–753, 1993.
Brennan, P. J.: Structure, function, and biogenesis of the cell wall of
Mycobacterium tuberculosis, Tuberculosis, 83, 91–97, 2003.
Brennan, P. J. and Nikaido, H.: The envelope of mycobacteria, Annu. Rev. Biochem., 64, 29–63, 1995.
Bull, I. D., Parekh, N. R., Hall, G. H., Ineson, P., and Evershed, R. P.:
Detection and classification of atmospheric methane oxidizing bacteria in
soil, Nature, 405, 175–1778, 2000.
Camacho-Ibar, V. F., Aveytua-Alcázar, L., and Carriquiry, J. D.: Fatty acid reactivities in sediment cores from the northern Gulf of California, Org. Geochem., 34, 425–439, 2003.
Caporaso, J. G., Lauber, C. L., Walters, W. A., Berg-Lyons, D., Huntley, J.,
Fierer, N., Owens, S. M., Betley, J., Fraser, L., and Bauer, M.:
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and
MiSeq platforms, The ISME journal, 6, 1621–1624, 2012.
Chou, S., Chedore, P., Haddad, A., Paul, N., and Kasatiya, S.: Direct
identification of Mycobacterium species in Bactec 7H12B medium by gas-liquid
chromatography, J. Clin. Microbiol., 34, 1317–1320, 1996.
Chou, S., Chedore, P., and Kasatiya, S.: Use of gas chromatographic fatty
acid and mycolic acid cleavage product determination to differentiate among
Mycobacterium genavense, Mycobacterium fortuitum, Mycobacterium simiae, and
Mycobacterium tuberculosis, J. Clin. Microbiol., 36, 577–579, 1998.
Christie, W. W.: Gas chromatography-mass spectrometry methods for structural
analysis of fatty acids, Lipids, 33, 343–353, 1998.
Coleman, N. V., Yau, S., Wilson, N. L., Nolan, L. M., Migocki, M. D., Ly, M.
a., Crossett, B., and Holmes, A. J.: Untangling the multiple monooxygenases
of Mycobacterium chubuense strain NBB4, a versatile hydrocarbon degrader,
Env. Microbiol. Rep., 3, 297–307, 2011.
Coleman, N. V., Le, N. B., Ly, M. A., Ogawa, H. E., Mc Carl, V., Wilson, N.
L., and Holmes, A. J.: Hydrocarbon monooxygenase in Mycobacterium:
recombinant expression of a member of the ammonia monooxygenase superfamily,
The ISME journal, 6, 171–182, 2012.
Crossman, Z., Ineson, P., and Evershed, R.: The use of 13C labelling of bacterial lipids in the characterisation of ambient methane-oxidising bacteria in soils, Org. Geochem., 36, 769–778, 2005.
Daffé, M. and Laneelle, M.: Distribution of phthiocerol diester,
phenolic mycosides and related compounds in mycobacteria, Microbiology, 134,
2049–2055, 1988.
Daffé, M., Quémard, A., and Marrakchi, H.: Mycolic Acids: From Chemistry to Biology, in: Biogenesis of Fatty Acids, Lipids and Membranes, Springer International Publishing, 181–216, https://doi.org/10.1007/978-3-319-50430-8_18, 2019.
Davis, J., Chase, H., and Raymond, R.: Mycobacterium paraffinicum n. sp., a
bacterium isolated from soil, Appl. Microbiol., 4, 310–315, 1956.
Davis, J., Raymond, R., and Stanley, J.: Areal contrasts in the abundance of
hydrocarbon oxidizing microbes in soils, Appl. Microbiol., 7, 156–165, 1959.
Dedysh, S. N., Belova, S. E., Bodelier, P. L., Smirnova, K. V., Khmelenina,
V. N., Chidthaisong, A., Trotsenko, Y. A., Liesack, W., and Dunfield, P. F.:
Methylocystis heyeri sp. nov., a novel type II methanotrophic bacterium
possessing “signature” fatty acids of type I methanotrophs, Int. J. Syst. Evol. Micr., 57, 472–479, 2007.
Delgado-Baquerizo, M., Oliverio, A. M., Brewer, T. E.,
Benavent-González, A., Eldridge, D. J., Bardgett, R. D., Maestre, F. T.,
Singh, B. K., and Fierer, N.: A global atlas of the dominant bacteria found
in soil, Science, 359, 320–325, 2018.
Donoghue, H., Taylor, G., Stewart, G., Lee, O., Wu, H., Besra, G., and
Minnikin, D.: Positive diagnosis of ancient leprosy and tuberculosis using
ancient DNA and lipid biomarkers, Diversity, 9, 46, https://doi.org/10.3390/d9040046, 2017.
Dworkin, M. and Foster, J.: Experiments with some microorganisms which
utilize ethane and hydrogen, J. Bacteriol., 75, 592–603, 1958.
Edgar, R. C.: MUSCLE: multiple sequence alignment with high accuracy and
high throughput, Nucleic Acids Res., 32, 1792–1797, 2004.
Edgar, R. C.: Search and clustering orders of magnitude faster than BLAST,
Bioinformatics, 26, 2460–2461, 2010.
Etiope, G., Caracausi, A., Favara, R., Italiano, F., and Baciu, C.: Methane
emission from the mud volcanoes of Sicily (Italy), Geophys. Res. Lett., 29, 56-51–56-54, 2002.
Etiope, G., Martinelli, G., Caracausi, A., and Italiano, F.: Methane seeps
and mud volcanoes in Italy: gas origin, fractionation and emission to the
atmosphere, Geophys. Res. Lett., 34, L14303, https://doi.org/10.1029/2007GL030341, 2007.
Falkinham, J. O.: The biology of environmental mycobacteria, Env. Microbiol. Rep., 1, 477–487, 2009.
Falkinham, J. O.: Environmental sources of nontuberculous mycobacteria,
Clin. Chest Med., 36, 35–41, 2015.
Farrimond, P., Griffiths, T., and Evdokiadis, E.: Hopanoic acids in Mesozoic
sedimentary rocks: their origin and relationship with hopanes, Org.
Geochem., 33, 965–977, 2002.
Fernandes, N. D. and Kolattukudy, P. E.: Methylmalonyl coenzyme A
selectivity of cloned and expressed acyltransferase and beta-ketoacyl
synthase domains of mycocerosic acid synthase from Mycobacterium bovis BCG,
J. Bacteriol., 179, 7538–7543, 1997.
Fierer, N., Leff, J. W., Adams, B. J., Nielsen, U. N., Bates, S. T., Lauber,
C. L., Owens, S., Gilbert, J. A., Wall, D. H., and Caporaso, J. G.:
Cross-biome metagenomic analyses of soil microbial communities and their
functional attributes, P. Natl. Acad. Sci. USA, 109, 21390–21395, 2012.
Francis, G. W.: Alkylthiolation for the determination of double-bond
position in unsaturated fatty acid esters, Chem. Phys. Lipids, 29, 369–374, 1981.
Frostegård, Å., Tunlid, A., and Bååth, E.: Use and misuse of
PLFA measurements in soils, Soil Biol. Biochem., 43, 1621–1625, 2011.
Gago, G., Diacovich, L., Parabolize, A., Tsai, S.-C., and Gramajo, H.: Fatty
acid biosynthesis in actinomycetes, FEMS Microbiol. Rev., 35, 475–497, 2011.
Grassa, F., Capasso, G., Favara, R., Inguaggiato, S., Faber, E., and
Valenza, M.: Molecular and isotopic composition of free hydrocarbon gases
from Sicily, Italy, Geophys. Res. Lett., 31, L06607, https://doi.org/10.1029/2003GL019362, 2004.
Hamieh, A., Tayyar, R., Tabaja, H., EL Zein, S., Bou Khalil, P., Kara, N.,
Kanafani, Z. A., Kanj, N., Bou Akl, I., and Araj, G.: Emergence of
Mycobacterium simiae: A retrospective study from a tertiary care center in
Lebanon, PloS One, 13, e0195390, https://doi.org/10.1371/journal.pone.0195390, 2018.
Harvey, D. J.: Picolinyl esters for the structural determination of fatty
acids by GC/MS, Mol. Biotechnol., 10, 251–260, 1998.
Heap, B.: Mycobacterium simiae as a cause of intra-abdominal disease: a case
report, Tubercle, 70, 217–221, 1989.
Hennessee, C. T., Seo, J.-S., Alvarez, A. M., and Li, Q. X.: Polycyclic
aromatic hydrocarbon-degrading species isolated from Hawaiian soils:
Mycobacterium crocinum sp. nov., Mycobacterium pallens sp. nov.,
Mycobacterium rutilum sp. nov., Mycobacterium rufum sp. nov. and
Mycobacterium aromaticivorans sp. nov, Int. J. Syst. Evol. Micr., 59, 378–387, 2009.
Holzheimer, M., Reijneveld, J. F., Ramnarine, A. K., Misiakos, G., Young, D.
C., Ishikawa, E., Cheng, T.-Y., Yamasaki, S., Moody, D. B., Van Rhijn, I.
and Minnaard A. J.: Asymmetric Total Synthesis of Mycobacterial Diacyl
Trehaloses Demonstrates a Role for Lipid Structure in Immunogenicity, ACS
Chem. Biol., 7, 1835–1841, 2020.
Huang, Y., Bol, R., Harkness, D. D., Ineson, P., and Eglinton, G.:
Post-glacial variations in distributions, 13C and 14C contents of
aliphatic hydrocarbons and bulk organic matter in three types of British
acid upland soils, Org. Geochem., 24, 273–287, 1996.
Inglis, G. N., Naafs, B. D. A., Zheng, Y., Mc Clymont, E. L., Evershed, R.
P., and Pancost, R. D.: Distributions of geohopanoids in peat: Implications
for the use of hopanoid-based proxies in natural archives, Geochim. Cosmochim. Ac., 224, 249–261, 2018.
Inglis, G. N., Naafs, B. D. A., Zheng, Y., Schellekens, J., and Pancost, R.
D.: δ13C values of bacterial hopanoids and leaf waxes as
tracers for methanotrophy in peatlands, Geochim. Cosmochim. Ac., 260, 244–256, 2019.
Jackson, M., Stadthagen, G., and Gicquel, B.: Long-chain multiple
methyl-branched fatty acid-containing lipids of Mycobacterium tuberculosis:
biosynthesis, transport, regulation and biological activities, Tuberculosis,
87, 78–86, 2007.
Jahnke, L. L., Summons, R. E., Hope, J. M., and Des Marais, D. J.: Carbon
isotopic fractionation in lipids from methanotrophic bacteria II: The
effects of physiology and environmental parameters on the biosynthesis and
isotopic signatures of biomarkers, Geochim. Cosmochim. Ac., 63, 79–93, 1999.
Kweon, O., Kim, S.-J., Blom, J., Kim, S.-K., Kim, B.-S., Baek, D.-H., Park,
S. I., Sutherland, J. B., and Cerniglia, C. E.: Comparative functional
pan-genome analyses to build connections between genomic dynamics and
phenotypic evolution in polycyclic aromatic hydrocarbon metabolism in the
genus Mycobacterium,
BMC Evol. Biol., 15, 21, https://doi.org/10.1186/s12862-015-0302-8, 2015.
Lamb, D. C., Kelly, D. E., Manning, N. J., and Kelly, S. L.: A sterol
biosynthetic pathway in Mycobacterium, FEBS Lett., 437, 142–144, 1998.
Lee, O. Y., Wu, H. H., Donoghue, H. D., Spigelman, M., Greenblatt, C. L.,
Bull, I. D., Rothschild, B. M., Martin, L. D., Minnikin, D. E., and Besra,
G. S.: Mycobacterium tuberculosis complex lipid virulence factors preserved
in the 17,000-year-old skeleton of an extinct bison, Bison antiquus, PLoS ONE, 7, e41923, https://doi.org/10.1371/journal.pone.0041923, 2012.
Lévy-Frébault, V., Pangon, B., Buré, A., Katlama, C., Marche,
C., and David, H.: Mycobacterium simiae and Mycobacterium avium-M.
intracellulare mixed infection in acquired immune deficiency syndrome,
J. Clin. Microbiol., 25, 154–157, 1987.
Lough, A.: The chemistry and biochemistry of phytanic, pristanic and related
acids, Progress in the Chemistry of Fats and other Lipids, 14, 1–48, 1975.
Martin, K. E., Ozsvar, J., and Coleman, N. V.: SmoXYB1C1Z of Mycobacterium
sp. strain NBB4: a soluble methane monooxygenase (sMMO)-like enzyme, active
on C2 to C4 alkanes and alkenes, Appl. Environ. Microbiol., 80,
5801–5806, 2014.
Miller, C., Child, R., Hughes, J., Benscai, M., Der, J., Sims, R., and
Anderson, A.: Diversity of soil mycobacterium isolates from three sites that
degrade polycyclic aromatic hydrocarbons, J. Appl. Microbiol., 102, 1612–1624, 2007.
Minnikin, D., Dobson, G., Goodfellow, M., Magnusson, M., and Ridell, M.:
Distribution of some mycobacterial waxes based on the phthiocerol family,
Microbiology, 131, 1375–1381, 1985.
Minnikin, D., Besra, G., Bolton, R., Datta, A., Mallet, A., Sharif, A.,
Stanford, J., Ridell, M., and Magnusson, M.: Identification of the leprosy
bacillus and related mycobacteria by analysis of mycocerosate profiles, Ann. Soc. Belg. Med. Tr., 73, 25–34, 1993a.
Minnikin, D., Bolton, R., Hartmann, S., Besra, G., Jenkins, P., Mallet, A.,
Wilkins, E., Lawson, A., and Ridell, M.: An integrated procedure for the
direct detection of characteristic lipids in tuberculous patients, Ann. Soc. Belg. Med. Tr., 73, 13–24, 1993b.
Minnikin, D. E., Kremer, L., Dover, L. G., and Besra, G. S.: The
methyl-branched fortifications of Mycobacterium tuberculosis, Chem. Biol., 9, 545–553, 2002.
Nechaeva, N: Two species of methane oxidizing mycobacteria.
Mikrobiologiya, 18, 310–317, 1949 (English Translation: Associated
Technical Service, East Orange, NJ).
Nei, M. and Kumar, S.: Molecular evolution and phylogenetics, Oxford
University Press, ISBN: 0-19-513584-9, 2000.
Nichols, P. D., Guckert, J. B., and White, D. C.: Determination of
monosaturated fatty acid double-bond position and geometry for microbial
monocultures and complex consortia by capillary GC-MS of their dimethyl
disulphide adducts, J. Microbiol. Meth., 5, 49–55, 1986.
Nicoara, S. C., Minnikin, D. E., Lee, O. C., O'Sullivan, D. M., McNerney,
R., Pillinger, C. T., Wright, I. P., and Morgan, G. H.: Development and
optimization of a gas chromatography/mass spectrometry method for the
analysis of thermochemolytic degradation products of phthiocerol
dimycocerosate waxes found in Mycobacterium tuberculosis, Rapid
Commun. Mass Sp., 27, 2374–2382, 2013.
Ourisson, G., Albrecht, P., and Rohmer, M.: The hopanoids: palaeochemistry
and biochemistry of a group of natural products, Pure Appl. Chem., 51, 709–729, 1979.
Park, H., Lee, H., Ro, Y. T., and Kim, Y. M.: Identification and functional
characterization of a gene for the methanol: N, N′-dimethyl-4-nitrosoaniline oxidoreductase from Mycobacterium sp. strain JC1 (DSM 3803), Microbiology, 156, 463–471, 2010.
Park, S. W., Hwang, E. H., Park, H., Kim, J. A., Heo, J., Lee, K. H., Song,
T., Kim, E., Ro, Y. T., and Kim, S. W.: Growth of mycobacteria on carbon
monoxide and methanol, J. Bacteriol., 185, 142–147, 2003.
Peterse, F., Nicol, G. W., Schouten, S., and Damsté, J. S. S.: Influence
of soil pH on the abundance and distribution of core and intact polar
lipid-derived branched GDGTs in soil, Org. Geochem., 41, 1171–1175, 2010.
Podust, L. M., Poulos, T. L., and Waterman, M. R.: Crystal structure of
cytochrome P450 14α-sterol demethylase (CYP51) from Mycobacterium
tuberculosis in complex with azole inhibitors, P. Natl. Acad. Sci. USA, 98, 3068–3073, 2001.
Ran-Ressler, R. R., Lawrence, P., and Brenna, J. T.: Structural
characterization of saturated branched chain fatty acid methyl esters by
collisional dissociation of molecular ions generated by electron ionization,
J. Lipid Res., 53, 195–203, 2012.
Redman, J. E., Shaw, M. J., Mallet, A. I., Santos, A. L., Roberts, C. A.,
Gernaey, A. M., and Minnikin, D. E.: Mycocerosic acid biomarkers for the
diagnosis of tuberculosis in the Coimbra Skeletal Collection, Tuberculosis,
89, 267–277, 2009.
Reed, W. M. and Dugan, P. R.: Isolation and characterization of the
facultative methylotroph Mycobacterium ID-Y, Microbiology, 133, 1389–1395,
1987.
Řezanka, T. and Sigler, K.: Odd-numbered very-long-chain fatty acids
from the microbial, animal and plant kingdoms, Prog. Lipid Res., 48, 206–238, 2009.
Ries-Kautt, M. and Albrecht, P.: Hopane-derived triterpenoids in soils,
Chem. Geol., 76, 143–151, 1989.
Rohmer, M., Bouvier-Nave, P., and Ourisson, G.: Distribution of hopanoid
triterpenes in prokaryotes, Microbiology, 130, 1137–1150, 1984.
Schouten, S., Hopmans, E. C., Baas, M., Boumann, H., Standfest, S.,
Könneke, M., Stahl, D. A., and Sinninghe Damsté, J. S.: Intact
membrane lipids of “Candidatus Nitrosopumilus maritimus”, a cultivated
representative of the cosmopolitan mesophilic group I crenarchaeota, Appl.
Environ. Microb., 74, 2433–2440, 2008.
Sinninghe Damsté, J. S., Rijpstra, W. I. C., Schouten, S., Fuerst, J.
A., Jetten, M. S., and Strous, M.: The occurrence of hopanoids in
planctomycetes: implications for the sedimentary biomarker record, Org.
Geochem., 35, 561–566, 2004.
Sinninghe Damsté, J. S., Rijpstra, W. I. C., Dedysh, S. N., Foesel, B.
U., and Villanueva, L.: Pheno-and genotyping of hopanoid production in
Acidobacteria, Front. Microbiol., 8, 968, https://doi.org/10.3389/fmicb.2017.00968, 2017.
Sinninghe Damsté, J. S., Rijpstra, W. I. C., Foesel, B. U., Huber, K.
J., Overmann, J., Nakagawa, S., Kim, J. J., Dunfield, P. F., Dedysh, S. N.,
and Villanueva, L.: An overview of the occurrence of ether-and ester-linked
iso-diabolic acid membrane lipids in microbial cultures of the
Acidobacteria: Implications for brGDGT paleoproxies for temperature and pH,
Org. Geochem., 124, 63–76, 2018.
Staccioli, G., McMillan, N., Meli, A., and Bartolini, G.: Chemical
characterisation of a 45-million-year bark from Geodetic Hills fossil
forest, Axel Heiberg Island, Canada, Wood Sci. Technol., 36, 419–427, 2002.
Talbot, H. M., Mc Clymont, E. L., Inglis, G. N., Evershed, R. P., and
Pancost, R. D.: Origin and preservation of bacteriohopanepolyol signatures
in Sphagnum peat from Bissendorfer Moor (Germany), Org. Geochem., 97, 95–110, 2016.
Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S.: MEGA6:
molecular evolutionary genetics analysis version 6.0, Mol. Biol. Evol., 30, 2725–2729, 2013.
Thiel, V., Blumenberg, M., Pape, T., Seifert, R., and Michaelis, W.:
Unexpected occurrence of hopanoids at gas seeps in the Black Sea, Org.
Geochem., 34, 81–87, 2003.
Tiedje, J. M., Asuming-Brempong, S., Nüsslein, K., Marsh, T. L., and
Flynn, S. J.: Opening the black box of soil microbial diversity, Appl. Soil Ecol., 13, 109–122, 1999.
Torkko, P., Suomalainen, S., Iivanainen, E., Suutari, M., Paulin, L.,
Rudbäck, E., Tortoli, E., Vincent, V., Mattila, R., and Katila, M.-L.:
Characterization of Mycobacterium bohemicum isolated from human, veterinary,
and environmental sources, J. Clin. Microbiol., 39, 207–211, 2001.
Torkko, P., Suomalainen, S., Iivanainen, E., Tortoli, E., Suutari, M.,
Seppänen, J., Paulin, L., and Katila, M.-L.: Mycobacterium palustre sp.
nov., a potentially pathogenic, slowly growing mycobacterium isolated from
clinical and veterinary specimens and from Finnish stream waters,
Int. J. Syst. Evol. Micr., 52, 1519–1525, 2002.
Torkko, P., Katila, M.-L., and Kontro, M.: Gas-chromatographic lipid
profiles in identification of currently known slowly growing environmental
mycobacteria, J. Med. Microbiol., 52, 315–323, 2003.
Tortoli, E.: Microbiological features and clinical relevance of new species
of the genus Mycobacterium, Clin. Microbiol. Rev., 27, 727–752, 2014.
Trincianti, E., Frixa, A., and Sartorio, D.: Palynology and stratigraphic
characterization of subsurface sedimentary successions in the Sicanian and
Imerese Domains–Central Western Sicily, Rev. Palaeobot. Palyno., 218, 48–66, 2015.
Valero-Guillén, P., Martín-Luengo, F., Larsson, L., Jimenez, J.,
Juhlin, I., and Portaels, F.: Fatty and mycolic acids of Mycobacterium
malmoense, J. Clin. Microbiol., 26, 153–154, 1988.
van Winden, J. F., Talbot, H. M., Kip, N., Reichart, G.-J., Pol, A.,
McNamara, N. P., Jetten, M. S., Op den Camp, H. J., and Sinninghe
Damsté, J. S.: Bacteriohopanepolyol signatures as markers for
methanotrophic bacteria in peat moss, Geochim. Cosmochim. Ac., 77, 52–61, 2012.
van Winden, J. F., Talbot, H. M., Reichart, G.-J., McNamara, N. P.,
Benthien, A., and Sinninghe Damsté, J. S.: Influence of temperature on
the δ13C values and distribution of methanotroph-related hopanoids in Sphagnum-dominated peat bogs, Geobiology, 18, 497–507,
https://doi.org/10.1111/gbi.12389, 2020.
Walsh, C. M., Gebert, M. J., Delgado-Baquerizo, M., Maestre, F., and Fierer,
N.: A global survey of mycobacterial diversity in soil, Appl. Environ. Microb., 85, e01180-19, https://doi.org/10.1128/AEM.01180-19, 2019.
Weijers, J. W., Panoto, E., van Bleijswijk, J., Schouten, S., Rijpstra, W.
I. C., Balk, M., Stams, A. J., and Damste, J. S. S.: Constraints on the
biological source(s) of the orphan branched tetraether membrane lipids,
Geomicrobiol. J., 26, 402–414, 2009.
Wenger, L. M., Davis, C. L., and Isaksen, G. H.: Multiple controls on
petroleum biodegradation and impact on oil quality, SPE Reserv. Eval. Eng., 5, 375–383, 2002.
World Health Organization: World health statistics 2019: monitoring health
for the SDGs, sustainable development goals, World Health Organization, 120 pp., ISBN: 9241565705, 2019.
Zhang, J., Kobert, K., Flouri, T., and Stamatakis, A.: PEAR: a fast and
accurate Illumina Paired-End reAd mergeR, Bioinformatics, 30, 614–620, 2013.
Zundel, M. and Rohmer, M.: Prokaryotic triterpenoids: 1. 3β-Methylhopanoids from Acetobacter species and Methylococcus capsulatus, Eur. J. Biochem., 150, 23–27, 1985.
Short summary
Soils from an everlasting fire (gas seep) in Sicily, Italy, reveal high relative abundances of novel uncultivated mycobacteria and unique 13C-depleted mycocerosic acids (multi-methyl branched fatty acids) close to the main gas seep. Our results imply that mycocerosic acids in combination with their depleted δ13C values offer a new biomarker tool to study the role of soil mycobacteria as hydrocarbon consumers in the modern and past global carbon cycle.
Soils from an everlasting fire (gas seep) in Sicily, Italy, reveal high relative abundances of...
Altmetrics
Final-revised paper
Preprint