Articles | Volume 20, issue 11
https://doi.org/10.5194/bg-20-2065-2023
© Author(s) 2023. 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-20-2065-2023
© Author(s) 2023. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Distributions of bacteriohopanepolyols in lakes and coastal lagoons of the Azores Archipelago
Department of Marine Microbiology & Biogeochemistry, NIOZ Royal
Netherlands Institute for Sea Research, 1790 AB Den Burg, the Netherlands
Department of Earth, Environmental and Planetary Sciences, Brown
University, Providence, RI, USA
Ellen C. Hopmans
Department of Marine Microbiology & Biogeochemistry, NIOZ Royal
Netherlands Institute for Sea Research, 1790 AB Den Burg, the Netherlands
Danica Mitrović
Department of Marine Microbiology & Biogeochemistry, NIOZ Royal
Netherlands Institute for Sea Research, 1790 AB Den Burg, the Netherlands
Pedro M. Raposeiro
Centro de Investigação em Biodiversidade e Recursos
Genéticos, CIBIO, InBIO Laboratório Associado, BIOPOLIS Program in
Genomics, Biodiversity and Land Planning, Polo dos
Açores, Ponta Delgada, Portugal
UNESCO Chair – Land Within Sea: Biodiversity and Sustainability in Atlantic Islands, Departamento de Biologia, Faculdade de Ciências e Tecnologia, Universidade dos Açores,
Ponta Delgada, Açores, Portugal
Vítor Gonçalves
Centro de Investigação em Biodiversidade e Recursos
Genéticos, CIBIO, InBIO Laboratório Associado, BIOPOLIS Program in
Genomics, Biodiversity and Land Planning, Polo dos
Açores, Ponta Delgada, Portugal
UNESCO Chair – Land Within Sea: Biodiversity and Sustainability in Atlantic Islands, Departamento de Biologia, Faculdade de Ciências e Tecnologia, Universidade dos Açores,
Ponta Delgada, Açores, Portugal
Ana C. Costa
Centro de Investigação em Biodiversidade e Recursos
Genéticos, CIBIO, InBIO Laboratório Associado, BIOPOLIS Program in
Genomics, Biodiversity and Land Planning, Polo dos
Açores, Ponta Delgada, Portugal
UNESCO Chair – Land Within Sea: Biodiversity and Sustainability in Atlantic Islands, Departamento de Biologia, Faculdade de Ciências e Tecnologia, Universidade dos Açores,
Ponta Delgada, Açores, Portugal
Linda A. Amaral-Zettler
Department of Marine Microbiology & Biogeochemistry, NIOZ Royal
Netherlands Institute for Sea Research, 1790 AB Den Burg, the Netherlands
Department of Earth, Environmental and Planetary Sciences, Brown
University, Providence, RI, USA
Department of Freshwater and Marine Ecology, Institute for
Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, the
Netherlands
Laura Villanueva
Department of Marine Microbiology & Biogeochemistry, NIOZ Royal
Netherlands Institute for Sea Research, 1790 AB Den Burg, the Netherlands
Department of Earth Sciences, Utrecht University, Utrecht, the
Netherlands
Darci Rush
Department of Marine Microbiology & Biogeochemistry, NIOZ Royal
Netherlands Institute for Sea Research, 1790 AB Den Burg, the Netherlands
Related authors
Nora Richter, James M. Russell, Johanna Garfinkel, and Yongsong Huang
Clim. Past, 17, 1363–1383, https://doi.org/10.5194/cp-17-1363-2021, https://doi.org/10.5194/cp-17-1363-2021, 2021
Short summary
Short summary
We present a reconstruction of winter–spring temperatures developed using organic proxies preserved in well-dated lake sediments from southwest Iceland to assess seasonal temperature changes in the North Atlantic region over the last 2000 years. The gradual warming trend observed in our record is likely influenced by sea surface temperatures, which are sensitive to changes in ocean circulation and seasonal insolation, during the winter and spring season.
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.
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.
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.
Reint Fischer, Delphine Lobelle, Merel Kooi, Albert Koelmans, Victor Onink, Charlotte Laufkötter, Linda Amaral-Zettler, Andrew Yool, and Erik van Sebille
Biogeosciences, 19, 2211–2234, https://doi.org/10.5194/bg-19-2211-2022, https://doi.org/10.5194/bg-19-2211-2022, 2022
Short summary
Short summary
Since current estimates show that only about 1 % of the all plastic that enters the ocean is floating at the surface, we look at subsurface processes that can cause vertical movement of (micro)plastic. We investigate how modelled algal attachment and the ocean's vertical movement can cause particles to sink and oscillate in the open ocean. Particles can sink to depths of > 5000 m in regions with high wind intensity and mainly remain close to the surface with low winds and biological activity.
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.
Nora Richter, James M. Russell, Johanna Garfinkel, and Yongsong Huang
Clim. Past, 17, 1363–1383, https://doi.org/10.5194/cp-17-1363-2021, https://doi.org/10.5194/cp-17-1363-2021, 2021
Short summary
Short summary
We present a reconstruction of winter–spring temperatures developed using organic proxies preserved in well-dated lake sediments from southwest Iceland to assess seasonal temperature changes in the North Atlantic region over the last 2000 years. The gradual warming trend observed in our record is likely influenced by sea surface temperatures, which are sensitive to changes in ocean circulation and seasonal insolation, during the winter and spring season.
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.
Nadine T. Smit, Laura Villanueva, Darci Rush, Fausto Grassa, Caitlyn R. Witkowski, Mira Holzheimer, Adriaan J. Minnaard, Jaap S. Sinninghe Damsté, and Stefan Schouten
Biogeosciences, 18, 1463–1479, https://doi.org/10.5194/bg-18-1463-2021, https://doi.org/10.5194/bg-18-1463-2021, 2021
Short summary
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.
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
Bale, N. J., Rijpstra, W. I. C., Sahonero-Canavesi, D. X., Oshkin, I. Y.,
Belova, S. E., Dedysh, S. N., and Sinninghe Damsté, J. S.: Fatty Acid
and Hopanoid Adaption to Cold in the Methanotroph Methylovulum psychrotolerans, Front.
Microbiol., 10, 589, https://doi.org/10.3389/fmicb.2019.00589, 2019.
Bale, N. J., Ding, S., Hopmans, E. C., Arts, M. G. I., Villanueva, L.,
Boschman, C., Haas, A. F., Schouten, S., and Sinninghe Damsté, J. S.:
Lipidomics of Environmental Microbial Communities, I: Visualization of
Component Distributions Using Untargeted Analysis of High-Resolution Mass
Spectrometry Data, Front. Microbiol., 12, 659302, https://doi.org/10.3389/fmicb.2021.659302, 2021.
Bastviken, D., Cole, J. J., Pace, M. L., and Van de Bogert, M. C.: Fates of
methane from different lake habitats: Connecting whole-lake budgets and
CH4 emissions, J. Geophys. Res.-Biogeo., 113, G2,
https://doi.org/10.1029/2007JG000608, 2008.
Bligh, E. G. and Dyer, W. J.: A rapid method of total lipid extraction and
purification, Can. J. Biochem. Physiol., 37, 911–917,
https://doi.org/10.1139/o59-099, 1959.
Blumenberg, M., Krüger, M., Nauhaus, K., Talbot, H. M., Oppermann, B.
I., Seifert, R., Pape, T., and Michaelis, W.: Biosynthesis of hopanoids by
sulfate-reducing bacteria (genus Desulfovibrio), Environ. Microbiol., 8,
1220–1227, https://doi.org/10.1111/j.1462-2920.2006.01014.x, 2006.
Blumenberg, M., Seifert, R., Kasten, S., Bahlmann, E., and Michaelis, W.:
Euphotic zone bacterioplankton sources major sedimentary
bacteriohopanepolyols in the Holocene Black Sea, Geochim. Cosmochim.
Ac., 73, 750–766, https://doi.org/10.1016/j.gca.2008.11.005, 2009.
Blumenberg, M., Hoppert, M., Krüger, M., Dreier, A., and Thiel, V.:
Novel findings on hopanoid occurrences among sulfate reducing bacteria: Is
there a direct link to nitrogen fixation?, Org. Geochem., 49, 1–5,
https://doi.org/10.1016/j.orggeochem.2012.05.003, 2012.
Blumenberg, M., Berndmeyer, C., Moros, M., Muschalla, M., Schmale, O., and
Thiel, V.: Bacteriohopanepolyols record stratification, nitrogen fixation
and other biogeochemical perturbations in Holocene sediments of the central
Baltic Sea, Biogeosciences, 10, 2725–2735,
https://doi.org/10.5194/bg-10-2725-2013, 2013.
Bradley, A. S., Pearson, A., Sáenz, J. P., and Marx, C. J.:
Adenosylhopane: The first intermediate in hopanoid side chain biosynthesis,
Org. Geochem., 41, 1075–1081,
https://doi.org/10.1016/j.orggeochem.2010.07.003, 2010.
Bravo, J.-M., Perzl, M., Härtner, T., Kannenberg, E. L., and Rohmer, M.:
Novel methylated triterpenoids of the gammacerane series from the
nitrogen-fixing bacterium Bradyrhizobium japonicum USDA 110, Eur. J. Biochem., 268,
1323–1331, https://doi.org/10.1046/j.1432-1327.2001.01998.x, 2001.
Cooke, M. P., Talbot, H. M., and Farrimond, P.: Bacterial populations
recorded in bacteriohopanepolyol distributions in soils from Northern
England, Org. Geochem., 39, 1347–1358,
https://doi.org/10.1016/j.orggeochem.2008.05.003, 2008.
Cooke, M. P., van Dongen, B. E., Talbot, H. M., Semiletov, I., Shakhova, N.,
Guo, L., and Gustafsson, Ö.: Bacteriohopanepolyol biomarker composition
of organic matter exported to the Arctic Ocean by seven of the major Arctic
rivers, Org. Geochem., 40, 1151–1159,
https://doi.org/10.1016/j.orggeochem.2009.07.014, 2009.
Coolen, M. J. L., Talbot, H. M., Abbas, B. A., Ward, C., Schouten, S.,
Volkman, J. K., and Sinninghe Damsté, J. S.: Sources for sedimentary
bacteriohopanepolyols as revealed by 16S rDNA stratigraphy, Environ.
Microbiol., 10, 1783–1803,
https://doi.org/10.1111/j.1462-2920.2008.01601.x, 2008.
Cordeiro, R., Luz, R., Vilaverde, J., Vasconcelos, V., Fonseca, A., and
Gonçalves, V.: Distribution of Toxic Cyanobacteria in Volcanic Lakes of
the Azores Islands, Water, 12, 3385, https://doi.org/10.3390/w12123385,
2020.
Cvejic, J. H., Bodrossy, L., Kovács, K. L., and Rohmer, M.: Bacterial
triterpenoids of the hopane series from the methanotrophic bacteria
Methylocaldum spp.: phylogenetic implications and first evidence for an unsaturated
aminobacteriohopanepolyol, FEMS Microbiol. Lett., 182, 361–365,
https://doi.org/10.1111/j.1574-6968.2000.tb08922.x, 2000.
De Jonge, C., Talbot, H. M., Bischoff, J., Stadnitskaia, A., Cherkashov, G.,
and Sinninghe Damsté, J. S.: Bacteriohopanepolyol distribution in
Yenisei River and Kara Sea suspended particulate matter and sediments traces
terrigenous organic matter input, Geochim. Cosmochim. Ac., 174,
85–101, https://doi.org/10.1016/j.gca.2015.11.008, 2016.
Doðrul Selver, A., Talbot, H. M., Gustafsson, Ö., Boult, S., and van
Dongen, B. E.: Soil organic matter transport along an sub-Arctic river–sea
transect, Org. Geochem., 51, 63–72,
https://doi.org/10.1016/j.orggeochem.2012.08.002, 2012.
Doðrul Selver, A., Sparkes, R. B., Bischoff, J., Talbot, H. M.,
Gustafsson, Ö., Semiletov, I. P., Dudarev, O. V., Boult, S., and van
Dongen, B. E.: Distributions of bacterial and archaeal membrane lipids in
surface sediments reflect differences in input and loss of terrestrial
organic carbon along a cross-shelf Arctic transect, Org. Geochem.,
83/84, 16–26, https://doi.org/10.1016/j.orggeochem.2015.01.005, 2015.
Doughty, D. M., Coleman, M. L., Hunter, R. C., Sessions, A. L., Summons, R.
E., and Newman, D. K.: The RND-family transporter, HpnN, is required for
hopanoid localization to the outer membrane of Rhodopseudomonas palustris TIE-1, P.
Natl. Acad. Sci. USA, 108, E1045–E1051,
https://doi.org/10.1073/pnas.1104209108, 2011.
Elling, F. J., Evans, T. W., Nathan, V., Hemingway, J. D., Kharbush, J. J.,
Bayer, B., Spieck, E., Husain, F., Summons, R. E., and Pearson, A.: Marine
and terrestrial nitrifying bacteria are sources of diverse
bacteriohopanepolyols, Geobiology, 20, 399–420,
https://doi.org/10.1111/gbi.12484, 2022.
Farrimond, P., Head, I. M., and Innes, H. E.: Environmental influence on the
biohopanoid composition of recent sediments, Geochim. Cosmochim.
Ac., 64, 2985–2992, https://doi.org/10.1016/S0016-7037(00)00404-X, 2000.
Gonçalves, V.: Contribuição do estudo das microalgas para a
avaliação da qualidade ecológica das lagoas dos Açores:
fitoplâncton e diatomáceas bentónicas, PhD thesis, University of the Azores,
Ponta Delgada, 343 pp., 2008.
Gonçalves, V., Raposeiro, P. M., Marques, H. S., Vilaverde, J., Balibrea,
A., Rosa, F., Sixto, M., and Costa, A. C.: Monitorização das Massas
de Água Interiores e de Transição da Região Hidrográfica
dos Açores. Relatório Anual do Ano 3 (R5/Ano 3) Ponta Delgada, University of the Azores, 2018.
Guggenheim, C., Freimann, R., Mayr, M. J., Beck, K., Wehrli, B., and
Bürgmann, H.: Environmental and Microbial Interactions Shape
Methane-Oxidizing Bacterial Communities in a Stratified Lake, Front. Microbiol., 11, 579427, https://doi.org/10.3389/fmicb.2020.579427, 2020.
Hanson, R. S.: Ecology and Diversity of Methylotrophic Organisms, in:
Advances in Applied Microbiology, vol. 26, edited by: Perlman, D., Academic
Press, 3–39, https://doi.org/10.1016/S0065-2164(08)70328-9, 1980.
Hanson, R. S. and Hanson, T. E.: Methanotrophic bacteria, Microbiol.
Rev., 60, 439–471, https://doi.org/10.1128/mr.60.2.439-471.1996, 1996.
Harrits, S. M. and Hanson, R. S.: Stratification of aerobic
methane-oxidizing organisms in Lake Mendota, Madison, Wisconsin, Limnol.
Oceanogr., 25, 412–421, https://doi.org/10.4319/lo.1980.25.3.0412,
1980.
Hernández, A., Kutiel, H., Trigo, R. M., Valente, M. A., Sigró, J.,
Cropper, T., and Santo, F. E.: New Azores archipelago daily precipitation
dataset and its links with large-scale modes of climate variability,
Int. J. Climatol., 36, 4439–4454,
https://doi.org/10.1002/joc.4642, 2016.
Hopmans, E. C., Smit, N. T., Schwartz-Narbonne, R., Sinninghe Damsté, J.
S., and Rush, D.: Analysis of non-derivatized bacteriohopanepolyols using
UHPLC-HRMS reveals great structural diversity in environmental lipid
assemblages, Org. Geochem., 160, 104285,
https://doi.org/10.1016/j.orggeochem.2021.104285, 2021.
Kusch, S. and Rush, D.: Revisiting the precursors of the most abundant
natural products on Earth: A look back at 30+ years of
bacteriohopanepolyol (BHP) research and ahead to new frontiers, Org. Geochem., 172, 104469, https://doi.org/10.1016/j.orggeochem.2022.104469,
2022.
Kusch, S., Sepúlveda, J., and Wakeham, S. G.: Origin of Sedimentary BHPs
Along a Mississippi River–Gulf of Mexico Export Transect: Insights From
Spatial and Density Distributions, Front. Mar. Sci., 6, 729, https://doi.org/10.3389/fmars.2019.00729, 2019.
Kusch, S., Wakeham, S. G., Dildar, N., Zhu, C., and Sepúlveda, J.:
Bacterial and archaeal lipids trace chemo(auto)trophy along the redoxcline
in Vancouver Island fjords, Geobiology, 19, 521–541,
https://doi.org/10.1111/gbi.12446, 2021a.
Kusch, S., Wakeham, S. G., and Sepúlveda, J.: Diverse origins of “soil
marker” bacteriohopanepolyols in marine oxygen deficient zones, Org. Geochem., 151, 104150, https://doi.org/10.1016/j.orggeochem.2020.104150,
2021b.
Matys, E. D., Sepúlveda, J., Pantoja, S., Lange, C. B., Caniupán,
M., Lamy, F., and Summons, R. E.: Bacteriohopanepolyols along redox
gradients in the Humboldt Current System off northern Chile, Geobiology, 15,
844–857, https://doi.org/10.1111/gbi.12250, 2017.
Meyers, P. A.: Preservation of elemental and isotopic source identification
of sedimentary organic matter, Chem. Geol., 114, 289–302,
https://doi.org/10.1016/0009-2541(94)90059-0, 1994.
Meyers, P. A.: Applications of organic geochemistry to paleolimnological
reconstructions: a summary of examples from the Laurentian Great Lakes,
Org. Geochem., 34, 261–289,
https://doi.org/10.1016/S0146-6380(02)00168-7, 2003.
Mitrović, D., Hopmans, E. C., Bale, N. J., Richter, N., Amaral-Zettler,
L. A., Baxter, A. J., Peterse, F., Miguel Raposeiro, P., Gonçalves, V.,
Cristina Costa, A., and Schouten, S.: Isoprenoidal GDGTs and GDDs associated
with anoxic lacustrine environments, Org. Geochem., 178, 104582,
https://doi.org/10.1016/j.orggeochem.2023.104582, 2023.
National Center for Biotechnology Information: PubChem Compound Summary for
CID 641496,
1,3-Oxazinan-2-one, https://pubchem.ncbi.nlm.nih.gov/compound/1_3-Oxazinan-2-one, last access: 26 January 2023a.
National Center for Biotechnology Information: PubChem Compound Summary for
CID 123834, 1,3-Dioxan-2-one,
https://pubchem.ncbi.nlm.nih.gov/compound/1_3-Dioxan-2-one,
last access: 26 January 2023b.
Neunlist, S. and Rohmer, M.: A novel hopanoid, 30-(5′-adenosyl)hopane, from
the purple non-sulphur bacterium Rhodopseudomonas acidophila, with possible DNA interactions, Biochem.
J., 228, 769–771, 1985a.
Neunlist, S. and Rohmer, M.: Novel hopanoids from the methylotrophic
bacteria Methylococcus capsulatus and Methylomonas methanica. (22S)-35-aminobacteriohopane-30,31,32,33,34-pentol and
(22S)-35-amino-3β-methylbacteriohopane-30,31,32,33,34-pentol,
Biochem. J., 231, 635–639, https://doi.org/10.1042/bj2310635,
1985b.
Neunlist, S. and Rohmer, M.: The Hopanoids of “Methylosinus trichosporium”: Aminobacteriohopanetriol
and Aminobacteriohopanetetrol, Microbiology, 131, 1363–1367,
https://doi.org/10.1099/00221287-131-6-1363, 1985c.
Neunlist, S., Bisseret, P., and Rohmer, M.: The hopanoids of the purple
non-sulfur bacteria Rhodopseudomonas palustris and Rhodopseudomonas acidophila and the absolute configuration of
bacteriohopanetetrol, Eur. J. Biochem., 171, 245–252,
https://doi.org/10.1111/j.1432-1033.1988.tb13783.x, 1988.
O'Beirne, M. D., Sparkes, R., Hamilton, T. L., van Dongen, B. E., Gilhooly,
W. P., and Werne, J. P.: Characterization of diverse bacteriohopanepolyols
in a permanently stratified, hyper-euxinic lake, Org. Geochem., 168,
104431, https://doi.org/10.1016/j.orggeochem.2022.104431, 2022.
Oksanen, J., Simpson, G., Blanchet, F., Kindt, R., Legendre, P., Minchin,
P., O'Hara, R., Solymos, P., Stevens, M., Szoecs, E., Wagner, H., Barbour,
M., Bedward, M., Bolker, B., Borcard, D., Carvalho, G., Chirico, M., De
Caceres, M., Durand, S., Evangelista, H., FitzJohn, R., Friendly, M.,
Furneaux, B., Hannigan, G., Hill, M., Lahti, L., McGlinn, D., Ouellette, M.,
Ribeiro Cunha, E., Smith, T., Stier, A., Ter Braak C., and Weedon J.:
vegan: Community Ecology Package R package
version 2.6-4,
https://CRAN.R-project.org/package=vegan (last access: 4 May 2023), 2022.
Osborne, K. A.: Environmental controls on bacteriohopanepolyol signatures in
estuarine sediments, Newcastle University, UK, PhD thesis, Newcastle University, http://theses.ncl.ac.uk/jspui/handle/10443/3214 (last access: 4 May 2023), 2015.
Osborne, K. A., Gray, N. D., Sherry, A., Leary, P., Mejeha, O., Bischoff,
J., Rush, D., Sidgwick, F. R., Birgel, D., Kalyuzhnaya, M. G., and Talbot,
H. M.: Methanotroph-derived bacteriohopanepolyol signatures as a function of
temperature related growth, survival, cell death and preservation in the
geological record, Environ. Microbiol. Rep., 9, 492–500,
https://doi.org/10.1111/1758-2229.12570, 2017.
Oswald, K., Milucka, J., Brand, A., Littmann, S., Wehrli, B., Kuypers, M. M.
M., and Schubert, C. J.: Light-Dependent Aerobic Methane Oxidation Reduces
Methane Emissions from Seasonally Stratified Lakes, PLOS ONE, 10, e0132574,
https://doi.org/10.1371/journal.pone.0132574, 2015.
Oswald, K., Milucka, J., Brand, A., Hach, P., Littmann, S., Wehrli, B.,
Kuypers, M. M. M., and Schubert, C. J.: Aerobic gammaproteobacterial
methanotrophs mitigate methane emissions from oxic and anoxic lake waters,
Limnol. Oceanogr., 61, S101–S118,
https://doi.org/10.1002/lno.10312, 2016.
Ourisson, G. and Albrecht, P.: Hopanoids, 1. Geohopanoids: the most abundant
natural products on Earth?, Acc. Chem. Res., 25, 398–402,
https://doi.org/10.1021/ar00021a003, 1992.
Pearson, A., Leavitt, W. D., Sáenz, J. P., Summons, R. E., Tam, M.
C.-M., and Close, H. G.: Diversity of hopanoids and squalene-hopene cyclases
across a tropical land-sea gradient, Environ. Microbiol., 11,
1208–1223, https://doi.org/10.1111/j.1462-2920.2008.01817.x, 2009.
Pereira, C. L., Raposeiro, P. M., Costa, A. C., Bao, R., Giralt, S., and
Gonçalves, V.: Biogeography and lake morphometry drive diatom and
chironomid assemblages' composition in lacustrine surface sediments of
oceanic islands, Hydrobiologia, 730, 93–112,
https://doi.org/10.1007/s10750-014-1824-6, 2014.
R Core Team: R: A language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, Austria, URL https://www.R-project.org/ (last access: 4 May 2023), 2023.
Raposeiro, P. M., Rubio, M. J., González, A., Hernández, A.,
Sánchez-López, G., Vázquez-Loureiro, D., Rull, V., Bao, R.,
Costa, A. C., Gonçalves, V., Sáez, A., and Giralt, S.: Impact of the
historical introduction of exotic fishes on the chironomid community of Lake
Azul (Azores Islands), Palaeogeogr. Palaeocl.,
466, 77–88, https://doi.org/10.1016/j.palaeo.2016.11.015, 2017.
Raposeiro, P. M., Saez, A., Giralt, S., Costa, A. C., and Gonçalves, V.:
Causes of spatial distribution of subfossil diatom and chironomid
assemblages in surface sediments of a remote deep island lake,
Hydrobiologia, 815, 141–163, https://doi.org/10.1007/s10750-018-3557-4,
2018.
Rethemeyer, J., Schubotz, F., Talbot, H. M., Cooke, M. P., Hinrichs, K.-U.,
and Mollenhauer, G.: Distribution of polar membrane lipids in permafrost
soils and sediments of a small high Arctic catchment, Org. Geochem.,
41, 1130–1145, https://doi.org/10.1016/j.orggeochem.2010.06.004, 2010.
Richter, N., Russell, J. M., Amaral-Zettler, L., DeGroff, W., Raposeiro, P.
M., Gonçalves, V., de Boer, E. J., Pla-Rabes, S., Hernández, A.,
Benavente, M., Ritter, C., Sáez, A., Bao, R., Trigo, R. M., Prego, R.,
and Giralt, S.: Long-term hydroclimate variability in the sub-tropical North
Atlantic and anthropogenic impacts on lake ecosystems: A case study from
Flores Island, the Azores, Quaternary Sci. Rev., 285, 107525,
https://doi.org/10.1016/j.quascirev.2022.107525, 2022.
Rohmer, M., Bouvier-Nave, P., and Ourisson, G. 1984: Distribution of
Hopanoid Triterpenes in Prokaryotes, Microbiology, 130, 1137–1150,
https://doi.org/10.1099/00221287-130-5-1137, 1984.
Rudd, J. W. M., Furutani, A., Flett, R. J., and Hamilton, R. D.: Factors
controlling methane oxidation in shield lakes: The role of nitrogen fixation
and oxygen concentration1, Limnol. Oceanogr., 21, 357–364,
https://doi.org/10.4319/lo.1976.21.3.0357, 1976.
Rush, D., Osborne, K. A., Birgel, D., Kappler, A., Hirayama, H., Peckmann,
J., Poulton, S. W., Nickel, J. C., Mangelsdorf, K., Kalyuzhnaya, M.,
Sidgwick, F. R., and Talbot, H. M.: The Bacteriohopanepolyol Inventory of
Novel Aerobic Methane Oxidising Bacteria Reveals New Biomarker Signatures of
Aerobic Methanotrophy in Marine Systems, PLOS ONE, 11, e0165635,
https://doi.org/10.1371/journal.pone.0165635, 2016.
Rush, D., Talbot, H. M., van der Meer, M. T. J., Hopmans, E. C., Douglas,
B., and Sinninghe Damsté, J. S.: Biomarker evidence for the occurrence
of anaerobic ammonium oxidation in the eastern Mediterranean Sea during
Quaternary and Pliocene sapropel formation, Biogeosciences, 16, 2467–2479,
https://doi.org/10.5194/bg-16-2467-2019, 2019.
Sáenz, J. P.: Hopanoid enrichment in a detergent resistant membrane
fraction of Crocosphaera watsonii: Implications for bacterial lipid raft formation, Org. Geochem., 41, 853–856,
https://doi.org/10.1016/j.orggeochem.2010.05.005, 2010.
Sáenz, J. P., Eglinton, T. I., and Summons, R. E.: Abundance and
structural diversity of bacteriohopanepolyols in suspended particulate
matter along a river to ocean transect, Org. Geochem., 42, 774–780,
https://doi.org/10.1016/j.orggeochem.2011.05.006, 2011.
Sáenz, J. P., Sezgin, E., Schwille, P., and Simons, K.: Functional
convergence of hopanoids and sterols in membrane ordering, P. Natl. Acad. Sci. USA, 109, 14236–14240,
https://doi.org/10.1073/pnas.1212141109, 2012.
Santos, F. D., Valente, M. A., Miranda, P. M. A., Aguiar, A., Azevedo, E.
B., Tomé, A. R., and Coelho, F.: Climate change scenarios in the Azores
and Madeira Islands, World Resour. Rev., 16, 473–491, 2004.
Seemann, M., Bisseret, P., Tritz, J.-P., Hooper, A. B., and Rohmer, M.:
Novel bacterial triterpenoids of the hopane series from Nitrosomonas europaea and their
significance for the formation of the C35 bacteriohopane skeleton,
Tetrahedron Lett., 40, 1681–1684,
https://doi.org/10.1016/S0040-4039(99)00064-7, 1999.
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.
Spencer-Jones, C. L., Wagner, T., Dinga, B. J., Schefuß, E., Mann, P.
J., Poulsen, J. R., Spencer, R. G. M., Wabakanghanzi, J. N., and Talbot, H.
M.: Bacteriohopanepolyols in tropical soils and sediments from the Congo
River catchment area, Org. Geochem., 89–90, 1–13,
https://doi.org/10.1016/j.orggeochem.2015.09.003, 2015.
Summons, R. E., Jahnke, L. L., Hope, J. M., and Logan, G. A.:
2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis,
Nature, 400, 554–557, https://doi.org/10.1038/23005, 1999.
Talbot, H. M. and Farrimond, P.: Bacterial populations recorded in diverse
sedimentary biohopanoid distributions, Org. Geochem., 38, 1212–1225,
https://doi.org/10.1016/j.orggeochem.2007.04.006, 2007.
Talbot, H. M., Watson, D. F., Murrell, J. C., Carter, J. F., and Farrimond,
P.: Analysis of intact bacteriohopanepolyols from methanotrophic bacteria by
reversed-phase high-performance liquid chromatography–atmospheric pressure
chemical ionisation mass spectrometry, J. Chromatogr. A, 921,
175–185, https://doi.org/10.1016/S0021-9673(01)00871-8, 2001.
Talbot, H. M., Watson, D. F., Pearson, E. J., and Farrimond, P.: Diverse
biohopanoid compositions of non-marine sediments, Org. Geochem., 34,
1353–1371, https://doi.org/10.1016/S0146-6380(03)00159-1, 2003.
Talbot, H. M., Rohmer, M., and Farrimond, P.: Rapid structural elucidation
of composite bacterial hopanoids by atmospheric pressure chemical ionisation
liquid chromatography/ion trap mass spectrometry, Rapid Commun.
Mass Sp., 21, 880–892, https://doi.org/10.1002/rcm.2911, 2007.
Talbot, H. M., Summons, R. E., Jahnke, L. L., Cockell, C. S., Rohmer, M.,
and Farrimond, P.: Cyanobacterial bacteriohopanepolyol signatures from
cultures and natural environmental settings, Org. Geochem., 39,
232–263, https://doi.org/10.1016/j.orggeochem.2007.08.006, 2008.
Talbot, H. M., Handley, L., Spencer-Jones, C. L., Dinga, B. J., Schefuß,
E., Mann, P. J., Poulsen, J. R., Spencer, R. G. M., Wabakanghanzi, J. N.,
and Wagner, T.: Variability in aerobic methane oxidation over the past
1.2Myrs recorded in microbial biomarker signatures from Congo fan sediments,
Geochim. Cosmochim. Ac., 133, 387–401,
https://doi.org/10.1016/j.gca.2014.02.035, 2014.
Talbot, H. M., Bischoff, J., Inglis, G. N., Collinson, M. E., and Pancost, R. D.: Polyfunctionalised bio- and geohopanoids in the Eocene Cobham Lignite, Org. Geochem., 96, 77–92, https://doi.org/10.1016/j.orggeochem.2016.03.006, 2016.
Taylor, K. A. and Harvey, H. R.: Bacterial hopanoids as tracers of organic
carbon sources and processing across the western Arctic continental shelf,
Org. Geochem., 42, 487–497,
https://doi.org/10.1016/j.orggeochem.2011.03.012, 2011.
Wagner, T., Kallweit, W., Talbot, H. M., Mollenhauer, G., Boom, A., and
Zabel, M.: Microbial biomarkers support organic carbon transport from
methane-rich Amazon wetlands to the shelf and deep sea fan during recent and
glacial climate conditions, Org. Geochem., 67, 85–98,
https://doi.org/10.1016/j.orggeochem.2013.12.003, 2014.
Watson, D. F. and Farrimond, P.: Novel polyfunctionalised geohopanoids in a
recent lacustrine sediment (Priest Pot, UK), Org. Geochem., 31,
1247–1252, https://doi.org/10.1016/S0146-6380(00)00148-0, 2000.
Welander, P. V. and Summons, R. E.: Discovery, taxonomic distribution, and
phenotypic characterization of a gene required for 3-methylhopanoid
production, P. Natl. Acad. Sci. USA, 109,
12905–12910, https://doi.org/10.1073/pnas.1208255109, 2012.
Welander, P. V., Hunter, R. C., Zhang, L., Sessions, A. L., Summons, R. E.,
and Newman, D. K.: Hopanoids Play a Role in Membrane Integrity and pH
Homeostasis in Rhodopseudomonas palustris TIE-1, J. Bacteriol., 191, 6145–6156,
https://doi.org/10.1128/JB.00460-09, 2009.
Welander, P. V., Coleman, M. L., Sessions, A. L., Summons, R. E., and
Newman, D. K.: Identification of a methylase required for 2-methylhopanoid
production and implications for the interpretation of sedimentary hopanes,
P. Natl. Acad. Sci. USA, 107, 8537–8542,
https://doi.org/10.1073/pnas.0912949107, 2010.
Whittenbury, R., Phillips, K. C., and Wilkinson, J. F.: Enrichment,
Isolation and Some Properties of Methane-utilizing Bacteria, J.
General Microbiol., 61, 205–218,
https://doi.org/10.1099/00221287-61-2-205, 1970.
Wickham, H.: ggplot2: Elegant Graphics for Data Analysis, Springer-Verlag
New York, ISBN 978-3-319-24277-4, https://ggplot2.tidyverse.org (last access: 4 May 2023), 2016.
van Grinsven, S., Sinninghe Damsté, J. S., Harrison, J., and Villanueva,
L.: Impact of Electron Acceptor Availability on Methane-Influenced
Microorganisms in an Enrichment Culture Obtained From a Stratified Lake,
Front. Microbiol., 11, 715, https://doi.org/10.3389/fmicb.2020.00715, 2020.
van Winden, J. F., Talbot, H. M., Kip, N., Reichart, G.-J., Pol, A.,
McNamara, N. P., Jetten, M. S. M., Op den Camp, H. J. M., and Sinninghe
Damsté, J. S.: Bacteriohopanepolyol signatures as markers for
methanotrophic bacteria in peat moss, Geochim. Cosmochim. Ac., 77,
52–61, https://doi.org/10.1016/j.gca.2011.10.026, 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 13C values and distribution of methanotroph-related hopanoids
in Sphagnum-dominated peat bogs, Geobiology, 18, 497–507,
https://doi.org/10.1111/gbi.12389, 2020.
Wang, M., Carver, J. J., Phelan, V. V., Sanchez, L. M., Garg, N., Peng, Y., Nguyen, D. D., Watrous, J., Kapono, C. A., Luzzatto-Knaan, T., Porto, C., Bouslimani, A., Melnik, A. V., Meehan, M. J., Liu, W.-T., Crüsemann, M., Boudreau, P. D., Esquenazi, E., Sandoval-Calderón, M., Kersten, R. D., Pace, L. A., Quinn, R. A., Duncan, K. R., Hsu, C.-C., Floros, D. J., Gavilan, R. G., Kleigrewe, K., Northen, T., Dutton, R. J., Parrot, D., Carlson, E. E., Aigle, B., Michelsen, C. F., Jelsbak, L., Sohlenkamp, C., Pevzner, P., Edlund, A., McLean, J., Piel, J., Murphy, B. T., Gerwick, L., Liaw, C.-C., Yang, Y.-L., Humpf, H.-U., Maansson, M., Keyzers, R. A., Sims, A. C., Johnson, A. R., Sidebottom, A. M., Sedio, B. E., Klitgaard, A., Larson, C. B., Boya P, C. A., Torres-Mendoza, D., Gonzalez, D. J., Silva, D. B., Marques, L. M., Demarque, D. P., Pociute, E., O’Neill, E. C., Briand, E., Helfrich, E. J. N., Granatosky, E. A., Glukhov, E., Ryffel, F., Houson, H., Mohimani, H., Kharbush, J. J., Zeng, Y., Vorholt, J. A., Kurita, K. L., Charusanti, P., McPhail, K. L., Nielsen, K. F., Vuong, L., Elfeki, M., Traxler, M. F., Engene, N., Koyama, N., Vining, O. B., Baric, R., Silva, R. R., Mascuch, S. J., Tomasi, S., Jenkins, S., Macherla, V., Hoffman, T., Agarwal, V., Williams, P. G., Dai, J., Neupane, R., Gurr, J., Rodríguez, A. M. C., Lamsa, A., Zhang, C., Dorrestein, K., Duggan, B. M., Almaliti, J., Allard, P.-M., et al.: Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking, Nat Biotechnol, 34, 828–837, https://doi.org/10.1038/nbt.3597, 2016 (data available at https://gnps.ucsd.edu/ProteoSAFe/static/gnps-splash.jsp, last access: 4 May 2023).
Xu, Y., Cooke, M. P., Talbot, H. M., and Simpson, M. J.:
Bacteriohopanepolyol signatures of bacterial populations in Western Canadian
soils, Org. Geochem., 40, 79–86,
https://doi.org/10.1016/j.orggeochem.2008.09.003, 2009.
Zhu, C., Talbot, H. M., Wagner, T., Pan, J.-M., and Pancost, R. D.:
Distribution of hopanoids along a land to sea transect: Implications for
microbial ecology and the use of hopanoids in environmental studies,
Limnol. Oceanogr., 56, 1850–1865,
https://doi.org/10.4319/lo.2011.56.5.1850, 2011.
Zindorf, M., Rush, D., Jaeger, J., Mix, A., Penkrot, M. L., Schnetger, B.,
Sidgwick, F. R., Talbot, H. M., van der Land, C., Wagner, T., Walczak, M.,
and März, C.: Reconstructing oxygen deficiency in the glacial Gulf of
Alaska: Combining biomarkers and trace metals as paleo-redox proxies,
Chem. Geol., 558, 119864,
https://doi.org/10.1016/j.chemgeo.2020.119864, 2020.
Zundel, M. and Rohmer, M.: Prokaryotic triterpenoids, Eur. J.
Biochem., 150, 23–27,
https://doi.org/10.1111/j.1432-1033.1985.tb08980.x, 1985.
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.
Bacteriohopanepolyols (BHPs) are a diverse class of lipids produced by bacteria across a wide...
Altmetrics
Final-revised paper
Preprint