Articles | Volume 20, issue 19
https://doi.org/10.5194/bg-20-4135-2023
© 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-20-4135-2023
© Author(s) 2023. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Research article
| 
09 Oct 2023
Research article |
| 09 Oct 2023
| 09 Oct 2023
Biogenic calcium carbonate as evidence for life
Sara Ronca
Department of Earth Sciences, Sapienza University of Rome, 00185, Rome, Italy
Francesco Mura
CNIS-Center for Nanotechnology Applied to Industry of La Sapienza,
Sapienza University of Rome, 00185, Rome, Italy
Marco Brandano
Department of Earth Sciences, Sapienza University of Rome, 00185, Rome, Italy
Angela Cirigliano
Istituto di Biologia e Patologia Molecolari, CNR, 00185, Rome, Italy
Francesca Benedetti
Department of Biology and Biotechnologies, Sapienza University of
Rome, 00185, Rome, Italy
Alessandro Grottoli
SARA ENViMOB Srl, 00171, Rome, Italy
Massimo Reverberi
Department of Environmental Biology, Sapienza University of Rome, 00185, Rome, Italy
Daniele Federico Maras
Soprintendenza Archeologia, Belle Arti e Paesaggio per la Provincia di
Viterbo e l'Etruria Meridionale, Ministero della Cultura, 00186, Rome, Italy
Rodolfo Negri
Department of Biology and Biotechnologies, Sapienza University of
Rome, 00185, Rome, Italy
Ernesto Di Mauro
Istituto di Biologia e Patologia Molecolari, CNR, 00185, Rome, Italy
Teresa Rinaldi
CORRESPONDING AUTHOR
Department of Biology and Biotechnologies, Sapienza University of
Rome, 00185, Rome, Italy
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Impact of seawater sulfate concentration on sulfur concentration and isotopic composition in calcite of two cultured benthic foraminifera
Marked recent declines in boron in Baltic Sea cod otoliths – a bellwether of incipient acidification in a vast hypoxic system?
The calcitic test growth rate of Spirillina vivipara (Foraminifera)
Ocean acidification enhances primary productivity and nocturnal carbonate dissolution in intertidal rock pools
Biomineralization of amorphous Fe-, Mn- and Si-rich mineral phases by cyanobacteria under oxic and alkaline conditions
Element ∕ Ca ratios in Nodosariida (Foraminifera) and their potential application for paleoenvironmental reconstructions
Deciphering the origin of dubiofossils from the Pennsylvanian of the Paraná Basin, Brazil
Properties of exopolymeric substances (EPSs) produced during cyanobacterial growth: potential role in whiting events
Inorganic component in oak waterlogged archaeological wood and volcanic lake compartments
Ultradian rhythms in shell composition of photosymbiotic and non-photosymbiotic mollusks
Extracellular enzyme activity in the coastal upwelling system off Peru: a mesocosm experiment
Multi-proxy assessment of brachiopod shell calcite as a potential archive of seawater temperature and oxygen isotope composition
Upper-ocean flux of biogenic calcite produced by the Arctic planktonic foraminifera Neogloboquadrina pachyderma
Do bacterial viruses affect framboid-like mineral formation?
Calcification response of reef corals to seasonal upwelling in the northern Arabian Sea (Masirah Island, Oman)
Growth rate rather than temperature affects the B∕Ca ratio in the calcareous red alga Lithothamnion corallioides
Heavy metal uptake of nearshore benthic foraminifera during multi-metal culturing experiments
A stable ultrastructural pattern despite variable cell size in Lithothamnion corallioides
Decoupling salinity and carbonate chemistry: low calcium ion concentration rather than salinity limits calcification in Baltic Sea mussels
Technical note: A universal method for measuring the thickness of microscopic calcite crystals, based on bidirectional circular polarization
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Kinetics of calcite precipitation by ureolytic bacteria under aerobic and anaerobic conditions
Coupled calcium and inorganic carbon uptake suggested by magnesium and sulfur incorporation in foraminiferal calcite
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Impact of salinity on element incorporation in two benthic foraminiferal species with contrasting magnesium contents
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Coral calcifying fluid aragonite saturation states derived from Raman spectroscopy
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Ba incorporation in benthic foraminifera
Size-dependent response of foraminiferal calcification to seawater carbonate chemistry
Technical note: an economical apparatus for the observation and harvest of mineral precipitation experiments with light microscopy
Caroline Thaler, Guillaume Paris, Marc Dellinger, Delphine Dissard, Sophie Berland, Arul Marie, Amandine Labat, and Annachiara Bartolini
Biogeosciences, 20, 5177–5198, https://doi.org/10.5194/bg-20-5177-2023, https://doi.org/10.5194/bg-20-5177-2023, 2023
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Our study focuses on one of the most used microfossils in paleoenvironmental reconstructions: foraminifera. We set up a novel approach of long-term cultures under variable and controlled conditions. Our results highlight that foraminiferal tests can be used as a unique record of both SO42−/CaCO3 and δ34S seawater variation. This establishes geological formations composed of biogenic carbonates as a potential repository of paleoenvironmental seawater sulfate chemical and geochemical variation.
Karin E. Limburg, Yvette Heimbrand, and Karol Kuliński
Biogeosciences, 20, 4751–4760, https://doi.org/10.5194/bg-20-4751-2023, https://doi.org/10.5194/bg-20-4751-2023, 2023
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We found a 3-to-5-fold decline in boron in Baltic cod otoliths between the late 1990s and 2021. The trend correlates with declines in oxygen and pH but not with increased salinity. Otolith B : Ca correlated with phosphorus in a healthy out-group (Icelandic cod) but not in Baltic cod. The otolith biomarkers Mn : Mg (hypoxia proxy) and B : Ca in cod otoliths suggest a general increase in both hypoxia and acidification within Baltic intermediate and deep waters in the last decade.
Yukiko Nagai, Katsuyuki Uematsu, Briony Mamo, and Takashi Toyofuku
EGUsphere, https://doi.org/10.5194/egusphere-2023-2259, https://doi.org/10.5194/egusphere-2023-2259, 2023
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This research highlights Spirillina vivipara's calcification strategy, highlighting variability in foraminiferal test formation. By examining its rapid growth and high calcification rate, we explain ecological strategies correlating with its broad coastal distribution. These insights amplify our understanding of foraminiferal ecology and underscore their impact on marine carbon cycling and paleoclimate studies, advocating for a species-specific approach in future research.
Narimane Dorey, Sophie Martin, and Lester Kwiatkowski
Biogeosciences, 20, 4289–4306, https://doi.org/10.5194/bg-20-4289-2023, https://doi.org/10.5194/bg-20-4289-2023, 2023
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Human CO2 emissions are modifying ocean carbonate chemistry, causing ocean acidification and likely already impacting marine ecosystems. Here, we added CO2 to intertidal pools at the start of emersion to investigate the influence of future ocean acidification on net community production (NCP) and calcification (NCC). By day, adding CO2 fertilized the pools (+20 % NCP). By night, pools experienced net community dissolution, a dissolution that was further increased (+40 %) by the CO2 addition.
Karim Benzerara, Agnès Elmaleh, Maria Ciobanu, Alexis De Wever, Paola Bertolino, Miguel Iniesto, Didier Jézéquel, Purificación López-García, Nicolas Menguy, Elodie Muller, Fériel Skouri-Panet, Sufal Swaraj, Rosaluz Tavera, Christophe Thomazo, and David Moreira
Biogeosciences, 20, 4183–4195, https://doi.org/10.5194/bg-20-4183-2023, https://doi.org/10.5194/bg-20-4183-2023, 2023
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Iron and manganese are poorly soluble in oxic and alkaline solutions but much more soluble under anoxic conditions. As a result, authigenic minerals rich in Fe and/or Mn have been viewed as diagnostic of anoxic conditions. However, here we reveal a new case of biomineralization by specific cyanobacteria, forming abundant Fe(III)- and Mn(IV)-rich amorphous phases under oxic conditions in an alkaline lake. This might be an overlooked biotic contribution to the scavenging of Fe from water columns.
Laura Pacho, Lennart de Nooijer, and Gert-Jan Reichart
Biogeosciences, 20, 4043–4056, https://doi.org/10.5194/bg-20-4043-2023, https://doi.org/10.5194/bg-20-4043-2023, 2023
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We analyzed Mg / Ca and other El / Ca (Na / Ca, B / Ca, Sr / Ca and Ba / Ca) in Nodosariata. Their calcite chemistry is markedly different to that of the other calcifying orders of foraminifera. We show a relation between the species average Mg / Ca and its sensitivity to changes in temperature. Differences were reflected in both the Mg incorporation and the sensitivities of Mg / Ca to temperature.
João Pedro Saldanha, Joice Cagliari, Rodrigo Scalise Horodyski, Lucas Del Mouro, and Mírian Liza Alves Forancelli Pacheco
Biogeosciences, 20, 3943–3979, https://doi.org/10.5194/bg-20-3943-2023, https://doi.org/10.5194/bg-20-3943-2023, 2023
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Marlisa Martinho de Brito, Irina Bundeleva, Frédéric Marin, Emmanuelle Vennin, Annick Wilmotte, Laurent Plasseraud, and Pieter T. Visscher
Biogeosciences, 20, 3165–3183, https://doi.org/10.5194/bg-20-3165-2023, https://doi.org/10.5194/bg-20-3165-2023, 2023
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Cyanobacterial blooms are associated with whiting events – natural occurrences of fine-grained carbonate precipitation in the water column. The role of organic matter (OM) produced by cyanobacteria in these events has been overlooked in previous research. Our laboratory experiments showed that OM affects the size and quantity of CaCO3 minerals. We propose a model of OM-associated CaCO3 precipitation during picoplankton blooms, which may have been neglected in modern and ancient events.
Giancarlo Sidoti, Federica Antonelli, Giulia Galotta, Maria Cristina Moscatelli, Davor Kržišnik, Vittorio Vinciguerra, Swati Tamantini, Rosita Marabottini, Natalia Macro, and Manuela Romagnoli
Biogeosciences, 20, 3137–3149, https://doi.org/10.5194/bg-20-3137-2023, https://doi.org/10.5194/bg-20-3137-2023, 2023
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The mineral content in archaeological wood pile dwellings and in the surrounding sediments in a volcanic lake was investigated. Calcium was the most abundant element; the second most abundant element was arsenic in sapwood. Sulfur, iron and potassium were also present. The mineral compounds are linked to the volcanic origin of the lake, to bioaccumulation processes induced by bacteria (i.e. sulfate-reducing bacteria) and to biochemical processes.
Niels J. de Winter, Daniel Killam, Lukas Fröhlich, Lennart de Nooijer, Wim Boer, Bernd R. Schöne, Julien Thébault, and Gert-Jan Reichart
Biogeosciences, 20, 3027–3052, https://doi.org/10.5194/bg-20-3027-2023, https://doi.org/10.5194/bg-20-3027-2023, 2023
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Mollusk shells are valuable recorders of climate and environmental changes of the past down to a daily resolution. To explore this potential, we measured changes in the composition of shells of two types of bivalves recorded at the hourly scale: the king scallop Pecten maximus and giant clams (Tridacna) that engaged in photosymbiosis. We find that photosymbiosis produces more day–night fluctuation in shell chemistry but that most of the variation is not periodic, perhaps recording weather.
Kristian Spilling, Jonna Piiparinen, Eric P. Achterberg, Javier Arístegui, Lennart T. Bach, Maria T. Camarena-Gómez, Elisabeth von der Esch, Martin A. Fischer, Markel Gómez-Letona, Nauzet Hernández-Hernández, Judith Meyer, Ruth A. Schmitz, and Ulf Riebesell
Biogeosciences, 20, 1605–1619, https://doi.org/10.5194/bg-20-1605-2023, https://doi.org/10.5194/bg-20-1605-2023, 2023
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We carried out an enclosure experiment using surface water off Peru with different additions of oxygen minimum zone water. In this paper, we report on enzyme activity and provide data on the decomposition of organic matter. We found very high activity with respect to an enzyme breaking down protein, suggesting that this is important for nutrient recycling both at present and in the future ocean.
Thomas Letulle, Danièle Gaspard, Mathieu Daëron, Florent Arnaud-Godet, Arnauld Vinçon-Laugier, Guillaume Suan, and Christophe Lécuyer
Biogeosciences, 20, 1381–1403, https://doi.org/10.5194/bg-20-1381-2023, https://doi.org/10.5194/bg-20-1381-2023, 2023
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This paper studies the chemistry of modern marine shells called brachiopods. We investigate the relationship of the chemistry of these shells with sea temperatures to test and develop tools for estimating sea temperatures in the distant past. Our results confirm that two of the investigated chemical markers could be useful thermometers despite some second-order variability independent of temperature. The other chemical markers investigated, however, should not be used as a thermometer.
Franziska Tell, Lukas Jonkers, Julie Meilland, and Michal Kucera
Biogeosciences, 19, 4903–4927, https://doi.org/10.5194/bg-19-4903-2022, https://doi.org/10.5194/bg-19-4903-2022, 2022
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This study analyses the production of calcite shells formed by one of the main Arctic pelagic calcifiers, the foraminifera N. pachyderma. Using vertically resolved profiles of shell concentration, size and weight, we show that calcification occurs throughout the upper 300 m with an average production flux below the calcification zone of 8 mg CaCO3 m−2 d−1 representing 23 % of the total pelagic biogenic carbonate production. The production flux is attenuated in the twilight zone by dissolution.
Paweł Działak, Marcin D. Syczewski, Kamil Kornaus, Mirosław Słowakiewicz, Łukasz Zych, and Andrzej Borkowski
Biogeosciences, 19, 4533–4550, https://doi.org/10.5194/bg-19-4533-2022, https://doi.org/10.5194/bg-19-4533-2022, 2022
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Bacteriophages comprise one of the factors that may influence mineralization processes. The number of bacteriophages in the environment usually exceeds the number of bacteria by an order of magnitude. One of the more interesting processes is the formation of framboidal pyrite, and it is not entirely clear what processes determine its formation. Our studies indicate that some bacterial viruses may influence the formation of framboid-like or spherical structures.
Philipp M. Spreter, Markus Reuter, Regina Mertz-Kraus, Oliver Taylor, and Thomas C. Brachert
Biogeosciences, 19, 3559–3573, https://doi.org/10.5194/bg-19-3559-2022, https://doi.org/10.5194/bg-19-3559-2022, 2022
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We investigate the calcification rate of reef corals from an upwelling zone, where low seawater pH and high nutrient concentrations represent a recent analogue for the future ocean. Calcification rate of the corals largely relies on extension growth. Variable responses of extension growth to nutrients either compensate or exacerbate negative effects of weak skeletal thickening associated with low seawater pH – a mechanism that is critical for the persistence of coral reefs under global change.
Giulia Piazza, Valentina A. Bracchi, Antonio Langone, Agostino N. Meroni, and Daniela Basso
Biogeosciences, 19, 1047–1065, https://doi.org/10.5194/bg-19-1047-2022, https://doi.org/10.5194/bg-19-1047-2022, 2022
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The coralline alga Lithothamnion corallioides is widely distributed in the Mediterranean Sea and NE Atlantic Ocean, where it constitutes rhodolith beds, which are diversity-rich ecosystems on the seabed. The boron incorporated in the calcified thallus of coralline algae (B/Ca) can be used to trace past changes in seawater carbonate and pH. This paper suggests a non-negligible effect of algal growth rate on B/Ca, recommending caution in adopting this proxy for paleoenvironmental reconstructions.
Sarina Schmidt, Ed C. Hathorne, Joachim Schönfeld, and Dieter Garbe-Schönberg
Biogeosciences, 19, 629–664, https://doi.org/10.5194/bg-19-629-2022, https://doi.org/10.5194/bg-19-629-2022, 2022
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The study addresses the potential of marine shell-forming organisms as proxy carriers for heavy metal contamination in the environment. The aim is to investigate if the incorporation of heavy metals is a direct function of their concentration in seawater. Culturing experiments with a metal mixture were carried out over a wide concentration range. Our results show shell-forming organisms to be natural archives that enable the determination of metals in polluted and pristine environments.
Valentina Alice Bracchi, Giulia Piazza, and Daniela Basso
Biogeosciences, 18, 6061–6076, https://doi.org/10.5194/bg-18-6061-2021, https://doi.org/10.5194/bg-18-6061-2021, 2021
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Ultrastructures of Lithothamnion corallioides, a crustose coralline alga collected from the Atlantic and Mediterranean Sea at different depths, show high-Mg-calcite cell walls formed by crystals with a specific shape and orientation that are unaffected by different environmental conditions of the living sites. This suggests that the biomineralization process is biologically controlled in coralline algae and can have interesting applications in paleontology.
Trystan Sanders, Jörn Thomsen, Jens Daniel Müller, Gregor Rehder, and Frank Melzner
Biogeosciences, 18, 2573–2590, https://doi.org/10.5194/bg-18-2573-2021, https://doi.org/10.5194/bg-18-2573-2021, 2021
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The Baltic Sea is expected to experience a rapid drop in salinity and increases in acidity and warming in the next century. Calcifying mussels dominate Baltic Sea seafloor ecosystems yet are sensitive to changes in seawater chemistry. We combine laboratory experiments and a field study and show that a lack of calcium causes extremely slow growth rates in mussels at low salinities. Subsequently, climate change in the Baltic may have drastic ramifications for Baltic seafloor ecosystems.
Luc Beaufort, Yves Gally, Baptiste Suchéras-Marx, Patrick Ferrand, and Julien Duboisset
Biogeosciences, 18, 775–785, https://doi.org/10.5194/bg-18-775-2021, https://doi.org/10.5194/bg-18-775-2021, 2021
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The coccoliths are major contributors to the particulate inorganic carbon in the ocean. They are extremely difficult to weigh because they are too small to be manipulated. We propose a universal method to measure thickness and weight of fine calcite using polarizing microscopy that does not require fine-tuning of the light or a calibration process. This method named "bidirectional circular polarization" uses two images taken with two directions of a circular polarizer.
Anna Piwoni-Piórewicz, Stanislav Strekopytov, Emma Humphreys-Williams, and Piotr Kukliński
Biogeosciences, 18, 707–728, https://doi.org/10.5194/bg-18-707-2021, https://doi.org/10.5194/bg-18-707-2021, 2021
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Calcifying organisms occur globally in almost every environment, and the process of biomineralization is of great importance in the global carbon cycle and use of skeletons as environmental data archives. The composition of skeletons is very complex. It is determined by the mechanisms of biological control on biomineralization and the response of calcifying organisms to varying environmental drivers. Yet for trace elements, such as Cu, Pb and Cd, an impact of environmental factors is pronounced.
Siham de Goeyse, Alice E. Webb, Gert-Jan Reichart, and Lennart J. de Nooijer
Biogeosciences, 18, 393–401, https://doi.org/10.5194/bg-18-393-2021, https://doi.org/10.5194/bg-18-393-2021, 2021
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Foraminifera are calcifying organisms that play a role in the marine inorganic-carbon cycle and are widely used to reconstruct paleoclimates. However, the fundamental process by which they calcify remains essentially unknown. Here we use inhibitors to show that an enzyme is speeding up the conversion between bicarbonate and CO2. This helps the foraminifera acquire sufficient carbon for calcification and might aid their tolerance to elevated CO2 level.
Anne Roepert, Lubos Polerecky, Esmee Geerken, Gert-Jan Reichart, and Jack J. Middelburg
Biogeosciences, 17, 4727–4743, https://doi.org/10.5194/bg-17-4727-2020, https://doi.org/10.5194/bg-17-4727-2020, 2020
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We investigated, for the first time, the spatial distribution of chlorine and fluorine in the shell walls of four benthic foraminifera species: Ammonia tepida, Amphistegina lessonii, Archaias angulatus, and Sorites marginalis. Cross sections of specimens were imaged using nanoSIMS. The distribution of Cl and F was co-located with organics in the rotaliids and rather homogeneously distributed in miliolids. We suggest that the incorporation is governed by the biomineralization pathway.
Vincent Mouchi, Camille Godbillot, Vianney Forest, Alexey Ulianov, Franck Lartaud, Marc de Rafélis, Laurent Emmanuel, and Eric P. Verrecchia
Biogeosciences, 17, 2205–2217, https://doi.org/10.5194/bg-17-2205-2020, https://doi.org/10.5194/bg-17-2205-2020, 2020
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Rare earth elements (REEs) in coastal seawater are included in bivalve shells during growth, and a regional fingerprint can be defined for provenance and environmental monitoring studies. We present a large dataset of REE abundances from oysters from six locations in France. The cupped oyster can be discriminated from one locality to another, but this is not the case for the flat oyster. Therefore, provenance studies using bivalve shells based on REEs are not adapted for the flat oyster.
Rosie L. Oakes and Jocelyn A. Sessa
Biogeosciences, 17, 1975–1990, https://doi.org/10.5194/bg-17-1975-2020, https://doi.org/10.5194/bg-17-1975-2020, 2020
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Pteropods are a group of tiny swimming snails whose fragile shells put them at risk from ocean acidification. We investigated the factors influencing the thickness of pteropods shells in the Cariaco Basin, off Venezuela, which is unaffected by ocean acidification. We found that pteropods formed thicker shells when nutrient concentrations, an indicator of food availability, were highest, indicating that food may be an important factor in mitigating the effects of ocean acidification on pteropods.
Miguel Gómez Batista, Marc Metian, François Oberhänsli, Simon Pouil, Peter W. Swarzenski, Eric Tambutté, Jean-Pierre Gattuso, Carlos M. Alonso Hernández, and Frédéric Gazeau
Biogeosciences, 17, 887–899, https://doi.org/10.5194/bg-17-887-2020, https://doi.org/10.5194/bg-17-887-2020, 2020
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In this paper, we assessed four methods (total alkalinity anomaly, calcium anomaly, 45Ca incorporation, and 13C incorporation) to determine coral calcification of a reef-building coral. Under all conditions (light vs. dark incubations and ambient vs. lowered pH levels), calcification rates estimated using the alkalinity and calcium anomaly techniques as well as 45Ca incorporation were highly correlated, while significantly different results were obtained with the 13C incorporation technique.
Alan Marron, Lucie Cassarino, Jade Hatton, Paul Curnow, and Katharine R. Hendry
Biogeosciences, 16, 4805–4813, https://doi.org/10.5194/bg-16-4805-2019, https://doi.org/10.5194/bg-16-4805-2019, 2019
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Isotopic signatures of silica fossils can be used as archives of past oceanic silicon cycling, which is linked to marine carbon uptake. However, the biochemistry that lies behind such chemical fingerprints remains poorly understood. We present the first measurements of silicon isotopes in a group of protists closely related to animals, choanoflagellates. Our results highlight a taxonomic basis to silica isotope signatures, possibly via a shared transport pathway in choanoflagellates and animals.
Laura M. Otter, Oluwatoosin B. A. Agbaje, Matt R. Kilburn, Christoph Lenz, Hadrien Henry, Patrick Trimby, Peter Hoppe, and Dorrit E. Jacob
Biogeosciences, 16, 3439–3455, https://doi.org/10.5194/bg-16-3439-2019, https://doi.org/10.5194/bg-16-3439-2019, 2019
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This study uses strontium as a trace elemental marker in combination with high-resolution nano-analytical techniques to label the growth fronts of bivalves in controlled aquaculture conditions. The growing shells incorporate the labels and are used as
snapshotsvisualizing the growth processes across different shell architectures. These observations are combined with structural investigations across length scales and altogether allow for a detailed understanding of this shell.
Simon Michael Ritter, Margot Isenbeck-Schröter, Christian Scholz, Frank Keppler, Johannes Gescher, Lukas Klose, Nils Schorndorf, Jerónimo Avilés Olguín, Arturo González-González, and Wolfgang Stinnesbeck
Biogeosciences, 16, 2285–2305, https://doi.org/10.5194/bg-16-2285-2019, https://doi.org/10.5194/bg-16-2285-2019, 2019
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Unique and spectacular under water speleothems termed as Hells Bells were recently reported from sinkholes (cenotes) of the Yucatán Peninsula, Mexico. However, the mystery of their formation remained unresolved. Here, we present detailed geochemical analyses and delineate that the growth of Hells Bells results from a combination of biogeochemical processes and variable hydraulic conditions within the cenote.
Andrew C. Mitchell, Erika J. Espinosa-Ortiz, Stacy L. Parks, Adrienne J. Phillips, Alfred B. Cunningham, and Robin Gerlach
Biogeosciences, 16, 2147–2161, https://doi.org/10.5194/bg-16-2147-2019, https://doi.org/10.5194/bg-16-2147-2019, 2019
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Microbially induced carbonate mineral precipitation (MICP) is a natural process that is also being investigated for subsurface engineering applications including radionuclide immobilization and microfracture plugging. We demonstrate that rates of MICP from microbial urea hydrolysis (ureolysis) vary with different bacterial strains, but rates are similar in both oxygenated and oxygen-free conditions. Ureolysis MICP is therefore a viable biotechnology in the predominately oxygen-free subsurface.
Inge van Dijk, Christine Barras, Lennart Jan de Nooijer, Aurélia Mouret, Esmee Geerken, Shai Oron, and Gert-Jan Reichart
Biogeosciences, 16, 2115–2130, https://doi.org/10.5194/bg-16-2115-2019, https://doi.org/10.5194/bg-16-2115-2019, 2019
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Systematics in the incorporation of different elements in shells of marine organisms can be used to test calcification models and thus processes involved in precipitation of calcium carbonates. On different scales, we observe a covariation of sulfur and magnesium incorporation in shells of foraminifera, which provides insights into the mechanics behind shell formation. The observed patterns imply that all species of foraminifera actively take up calcium and carbon in a coupled process.
Eveline M. Mezger, Lennart J. de Nooijer, Jacqueline Bertlich, Jelle Bijma, Dirk Nürnberg, and Gert-Jan Reichart
Biogeosciences, 16, 1147–1165, https://doi.org/10.5194/bg-16-1147-2019, https://doi.org/10.5194/bg-16-1147-2019, 2019
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Seawater salinity is an important factor when trying to reconstruct past ocean conditions. Foraminifera, small organisms living in the sea, produce shells that incorporate more Na at higher salinities. The accuracy of reconstructions depends on the fundamental understanding involved in the incorporation and preservation of the original Na of the shell. In this study, we unravel the Na composition of different components of the shell and describe the relative contribution of these components.
Hengchao Xu, Xiaotong Peng, Shijie Bai, Kaiwen Ta, Shouye Yang, Shuangquan Liu, Ho Bin Jang, and Zixiao Guo
Biogeosciences, 16, 949–960, https://doi.org/10.5194/bg-16-949-2019, https://doi.org/10.5194/bg-16-949-2019, 2019
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Viruses have been acknowledged as important components of the marine system for the past 2 decades, but understanding of their role in the functioning of the geochemical cycle remains poor. Results show viral lysis of cyanobacteria can influence the carbonate equilibrium system remarkably and promotes the formation and precipitation of carbonate minerals. Amorphous calcium carbonate (ACC) and aragonite are evident in the lysate, implying that different precipitation processes have occurred.
Nicole M. J. Geerlings, Eva-Maria Zetsche, Silvia Hidalgo-Martinez, Jack J. Middelburg, and Filip J. R. Meysman
Biogeosciences, 16, 811–829, https://doi.org/10.5194/bg-16-811-2019, https://doi.org/10.5194/bg-16-811-2019, 2019
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Multicellular cable bacteria form long filaments that can reach lengths of several centimeters. They affect the chemistry and mineralogy of their surroundings and vice versa. How the surroundings affect the cable bacteria is investigated. They show three different types of biomineral formation: (1) a polymer containing phosphorus in their cells, (2) a sheath of clay surrounding the surface of the filament and (3) the encrustation of a filament via a solid phase containing iron and phosphorus.
Facheng Ye, Hana Jurikova, Lucia Angiolini, Uwe Brand, Gaia Crippa, Daniela Henkel, Jürgen Laudien, Claas Hiebenthal, and Danijela Šmajgl
Biogeosciences, 16, 617–642, https://doi.org/10.5194/bg-16-617-2019, https://doi.org/10.5194/bg-16-617-2019, 2019
Yukiko Nagai, Katsuyuki Uematsu, Chong Chen, Ryoji Wani, Jarosław Tyszka, and Takashi Toyofuku
Biogeosciences, 15, 6773–6789, https://doi.org/10.5194/bg-15-6773-2018, https://doi.org/10.5194/bg-15-6773-2018, 2018
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We interpret detailed SEM and time-lapse observations of the calcification process in living foraminifera, which we reveal to be directly linked to the construction mechanism of organic membranes where the calcium carbonate precipitation takes place. We show that these membranes are a highly perforated outline is first woven by skeletal pseudopodia and then later overlaid by a layer of membranous pseudopodia to close the gaps. The chemical composition is related to these structures.
Agathe Martignier, Montserrat Filella, Kilian Pollok, Michael Melkonian, Michael Bensimon, François Barja, Falko Langenhorst, Jean-Michel Jaquet, and Daniel Ariztegui
Biogeosciences, 15, 6591–6605, https://doi.org/10.5194/bg-15-6591-2018, https://doi.org/10.5194/bg-15-6591-2018, 2018
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The unicellular microalga Tetraselmis cordiformis (Chlorophyta) was recently discovered to form intracellular mineral inclusions, called micropearls, which had been previously overlooked. The present study shows that 10 Tetraselmis species out of the 12 tested share this biomineralization capacity, producing amorphous calcium carbonate inclusions often enriched in Sr. This novel biomineralization process can take place in marine, brackish or freshwater and is therefore a widespread phenomenon.
Ulrike Braeckman, Felix Janssen, Gaute Lavik, Marcus Elvert, Hannah Marchant, Caroline Buckner, Christina Bienhold, and Frank Wenzhöfer
Biogeosciences, 15, 6537–6557, https://doi.org/10.5194/bg-15-6537-2018, https://doi.org/10.5194/bg-15-6537-2018, 2018
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Global warming has altered Arctic phytoplankton communities, with unknown effects on deep-sea communities that depend strongly on food produced at the surface. We compared the responses of Arctic deep-sea benthos to input of phytodetritus from diatoms and coccolithophorids. Coccolithophorid carbon was 5× less recycled than diatom carbon. The utilization of the coccolithophorid carbon may be less efficient, so a shift from diatom to coccolithophorid blooms could entail a delay in carbon cycling.
Hongrui Zhang, Heather Stoll, Clara Bolton, Xiaobo Jin, and Chuanlian Liu
Biogeosciences, 15, 4759–4775, https://doi.org/10.5194/bg-15-4759-2018, https://doi.org/10.5194/bg-15-4759-2018, 2018
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The sinking speeds of coccoliths are relevant for laboratory methods to separate coccoliths for geochemical analysis. However, in the absence of estimates of coccolith settling velocity, previous implementations have depended mainly on time-consuming method development by trial and error. In this study, the sinking velocities of cocooliths were carefully measured for the first time. We also provide an estimation of coccolith sinking velocity by shape, which will make coccolith separation easier.
Justin Michael Whitaker, Sai Vanapalli, and Danielle Fortin
Biogeosciences, 15, 4367–4380, https://doi.org/10.5194/bg-15-4367-2018, https://doi.org/10.5194/bg-15-4367-2018, 2018
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Materials, like soils or cements, can require repair. This study used a new bacterium (Sporosarcina ureae) in a repair method called "microbially induced carbonate precipitation" (MICP). In three trials, benefits were shown: S. ureae could make a model sandy soil much stronger by MICP, in fact better than a lot of other bacteria. However, MICP-treated samples got weaker in three trials of acid rain. In conclusion, S. ureae in MICP repair shows promise when used in appropriate climates.
Esmee Geerken, Lennart Jan de Nooijer, Inge van Dijk, and Gert-Jan Reichart
Biogeosciences, 15, 2205–2218, https://doi.org/10.5194/bg-15-2205-2018, https://doi.org/10.5194/bg-15-2205-2018, 2018
Jörn Thomsen, Kirti Ramesh, Trystan Sanders, Markus Bleich, and Frank Melzner
Biogeosciences, 15, 1469–1482, https://doi.org/10.5194/bg-15-1469-2018, https://doi.org/10.5194/bg-15-1469-2018, 2018
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The distribution of mussel in estuaries is limited but the mechanisms are not well understood. We document for the first time that reduced Ca2+ concentration in the low saline, brackish Baltic Sea affects the ability of mussel larvae to calcify the first larval shell. As complete formation of the shell is a prerequisite for successful development, impaired calcification during this sensitive life stage can have detrimental effects on the species' ability to colonize habitats.
Sha Ni, Isabelle Taubner, Florian Böhm, Vera Winde, and Michael E. Böttcher
Biogeosciences, 15, 1425–1445, https://doi.org/10.5194/bg-15-1425-2018, https://doi.org/10.5194/bg-15-1425-2018, 2018
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Spirorbis tube worms are common epibionts on brown algae in the Baltic Sea. We made experiments with Spirorbis in the
Kiel Outdoor Benthocosmsat CO2 and temperature conditions predicted for the year 2100. The worms were able to grow tubes even at CO2 levels favouring shell dissolution but did not survive at mean temperatures over 24° C. This indicates that Spirorbis worms will suffer from future excessive ocean warming and from ocean acidification fostering corrosion of their protective tubes.
Andrea C. Gerecht, Luka Šupraha, Gerald Langer, and Jorijntje Henderiks
Biogeosciences, 15, 833–845, https://doi.org/10.5194/bg-15-833-2018, https://doi.org/10.5194/bg-15-833-2018, 2018
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Calcifying phytoplankton play an import role in long-term CO2 removal from the atmosphere. We therefore studied the ability of a representative species to continue sequestrating CO2 under future climate conditions. We show that CO2 sequestration is negatively affected by both an increase in temperature and the resulting decrease in nutrient availability. This will impact the biogeochemical cycle of carbon and may have a positive feedback on rising CO2 levels.
Merinda C. Nash and Walter Adey
Biogeosciences, 15, 781–795, https://doi.org/10.5194/bg-15-781-2018, https://doi.org/10.5194/bg-15-781-2018, 2018
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Past seawater temperatures can be reconstructed using magnesium / calcium ratios of biogenic carbonates. As temperature increases, so does magnesium. Here we show that for these Arctic/subarctic coralline algae, anatomy is the first control on Mg / Ca, not temperature. When using coralline algae for temperature reconstruction, it is first necessary to check for anatomical influences on Mg / Ca.
Thomas M. DeCarlo, Juan P. D'Olivo, Taryn Foster, Michael Holcomb, Thomas Becker, and Malcolm T. McCulloch
Biogeosciences, 14, 5253–5269, https://doi.org/10.5194/bg-14-5253-2017, https://doi.org/10.5194/bg-14-5253-2017, 2017
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We present a new technique to quantify the chemical conditions under which corals build their skeletons by analysing them with lasers at a very fine resolution, down to 1/100th the width of a human hair. Our first applications to laboratory-cultured and wild corals demonstrates the complex interplay among seawater conditions (temperature and acidity), calcifying fluid chemistry, and bulk skeleton accretion, which will define the sensitivity of coral calcification to 21st century climate change.
Giulia Faucher, Linn Hoffmann, Lennart T. Bach, Cinzia Bottini, Elisabetta Erba, and Ulf Riebesell
Biogeosciences, 14, 3603–3613, https://doi.org/10.5194/bg-14-3603-2017, https://doi.org/10.5194/bg-14-3603-2017, 2017
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The main goal of this study was to understand if, similarly to the fossil record, high quantities of toxic metals induce coccolith dwarfism in coccolithophore species. We investigated, for the first time, the effects of trace metals on coccolithophore species other than E. huxleyi and on coccolith morphology and size. Our data show a species-specific sensitivity to trace metal concentration, allowing the recognition of the most-, intermediate- and least-tolerant taxa to trace metal enrichments.
Lennart J. de Nooijer, Anieke Brombacher, Antje Mewes, Gerald Langer, Gernot Nehrke, Jelle Bijma, and Gert-Jan Reichart
Biogeosciences, 14, 3387–3400, https://doi.org/10.5194/bg-14-3387-2017, https://doi.org/10.5194/bg-14-3387-2017, 2017
Michael J. Henehan, David Evans, Madison Shankle, Janet E. Burke, Gavin L. Foster, Eleni Anagnostou, Thomas B. Chalk, Joseph A. Stewart, Claudia H. S. Alt, Joseph Durrant, and Pincelli M. Hull
Biogeosciences, 14, 3287–3308, https://doi.org/10.5194/bg-14-3287-2017, https://doi.org/10.5194/bg-14-3287-2017, 2017
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It is still unclear whether foraminifera (calcifying plankton that play an important role in cycling carbon) will have difficulty in making their shells in more acidic oceans, with different studies often reporting apparently conflicting results. We used live lab cultures, mathematical models, and fossil measurements to test this question, and found low pH does reduce calcification. However, we find this response is likely size-dependent, which may have obscured this response in other studies.
Chris H. Crosby and Jake V. Bailey
Biogeosciences, 14, 2151–2154, https://doi.org/10.5194/bg-14-2151-2017, https://doi.org/10.5194/bg-14-2151-2017, 2017
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In the course of experiments exploring the formation of calcium phosphate minerals in a polymeric matrix, we developed a small-scale, reusable, and low-cost setup that allows microscopic observation over time for use in mineral precipitation experiments that use organic polymers as a matrix. The setup uniquely accommodates changes in solution chemistry during the course of an experiment and facilitates easy harvesting of the precipitates for subsequent analysis.
Cited articles
Allwood, A. C., Walter, M. R., Kamber, B. S., Marshall, C. P., and Burch,
I. W.: Stromatolite reef from the Early Archaean era of Australia, Nature,
441, 714–718, https://doi.org/10.1038/nature04764, 2006.
Anbu, P., Kang, C.-H., Shin, Y.-J., and So, J.-S.: Formations of calcium
carbonate minerals by bacteria and its multiple applications. SpringerPlus
5, 250, https://doi.org/10.1186/s40064-016-1869-2, 2016.
Asta, M. P., Fernandez-Martinez, A., Alonso, J., Charlet, L., Findling, N.,
Magnin, V., Ruta, B., Sprung, M., and Westermeier, F.: Nanoscale Ion
Dynamics Control on Amorphous Calcium Carbonate Crystallization: Precise
Control of Calcite Crystal Sizes, J. Phys. Chem. C., 124, 25645–25656,
https://doi.org/10.1021/acs.jpcc.0c08670, 2020.
Banerjee, S. and Joshi, S. R.: Ultrastructural analysis of calcite crystal
patterns formed by biofilm bacteria associated with cave speleothems,
Journal of Microscopy and Ultrastructure, 2, 217–223, 2014.
Banks, E. D., Taylor, N. M., Gulley, J., Lubbers, B. R., Giarrizzo, J. G.,
Bullen, H. A, Hoehler, T. M., and Barton, H. A.: Bacterial calcium carbonate
precipitation in cave environments: a function of calcium homeostasis,
Geomicrobiol. J., 27, 444–454,
https://doi.org/10.1080/01490450903485136, 2010.
Barton, H. A. and Northup, D. E.: Geomicrobiology in cave environments: past,
current and future perspectives, J. Cave Karst Stud., 69,
163–178, 2007.
Baskar, S., Baskar, R., and Routh, J.: Biogenic evidences of moonmilk
deposition in the Mawmluh cave, Meghalaya, India, Geomicrobiol. J.,
28, 252–265, https://doi.org/10.1080/01490451.2010.494096, 2011.
Benedetti, F., Kratter, M., Atanasio, P., Mura, F., Beccaccioli, M., Scifo, J., di Sarcina, I., Tomassetti, M. C., Schneider, K., Rossi, M., Cemmi, A., Nigro, L., and Rinaldi, T.: Isolation of carbonatogenic bacteria for biorestoration, J. Cult. Herit.,
in review, 2023.
Berg, B. L., Ronholm, J., Applin, D. M., Mann, P., Izawa, M., Cloutis, E. A.,
and Whyte, L. G.: Spectral features of biogenic calcium carbonates and
implications for astrobiology, Int. J. Astrobiol., 13, 353,
https://doi.org/10.1017/S1473550414000366, 2014.
Bizzarri, B. M., Saladino, R., Delfino, I., García-Ruiz, J. M., and Di
Mauro, E.: Prebiotic organic chemistry of formamide and the origin of life
in planetary conditions: What we know and what is the future, Int. J. Mol.
Sci., 22, 917, https://doi.org/10.3390/ijms22020917, 2021.
Blanco, A., Orofino, V., D'Elia, M., Fonti, S., Mastandrea, A., Guido, A.,
and Russo, F.: Infrared spectroscopy of microbially induced carbonates and
past life on Mars, Icarus, 226, 119–126,
https://doi.org/10.1016/j.icarus.2013.05.016, 2013.
Borsato, A., Frisia, S., Jones, B., and Van Der Borg, K.: Calcite moonmilk:
crystal morphology and environment of formation in caves in the Italian
Alps, J. Sediment. Res., 70, 1171–1182,
https://doi.org/10.1306/032300701171, 2000.
Boynton, W. V., Ming, D. W., Kounaves, S. P., Young, S. M. M., Arvidson, R. E.,
Hecht, M. H., Hoffman, J., Niles, P. B.; Hamara, D. K.; Quinn, R. C., Smith,
P. H., Sutter, B., Catling, D. C., and Morris, R. V.: Evidence for calcium
carbonate at the Mars Phoenix landing site, Science, 325, 61–64,
https://doi.10.1126/science.1172768, 2009.
Braissant, O., Bindschedler, S., Daniels, A. U., Verrecchia, E. P., and
Cailleau, G.: Microbiological activities in moonmilk monitored using
isothermal microcalorimetry (cave of vers chez le Brandt, Neuchatel,
Switzerland), J. Cave Karst Stud., 74, 116–126,
https://doi.org/10.4311/2011JCKS0213, 2012.
Bultel, B., Viennet, J. C., Poulet, F., Carter, J., and Werner, S. C.:
Detection of carbonates in Martian weathering profiles. J. Geophys. Res.-Sol. Ea., 124, 989–1007, https://doi.org/10.1029/2018JE005845, 2019.
Cacchio, P., Ferrini, G., Ercole, C., Del Gallo, M., and Lepidi, A.:
Biogenicity and characterization of moonmilk in the grotta nera (Majella
National Park, Abruzzi, Central Italy), J. Cave Karst Stud.,
76, 88, https://doi.org/10.4311/2012MB0275, 2014.
Cailleau, G., Verrecchia, E. P., Braissant, O., and Emmanuel, L.: The
biogenic origin of needle fiber calcite, Sedimentology, 56, 1858–1875,
https://doi.org/10.1111/j.1365-3091.2009.01060.x, 2009.
Cañaveras, J. C., Cuezva, S., Sanchez-Moral, S., Lario, J., Laiz, L.,
Gonzalez, J. M., and Saiz-Jimenez, C.: On the origin of fiber calcite
crystals in moonmilk deposits, Naturwissenschaften, 93, 27–32,
https://doi.org/10.1007/s00114-005-0052-3, 2006.
Changela, H. G., Chatzitheodoridis, E., Antunes, A., Beaty, D., Bouw, K.,
Bridges, J. C., Capova, K. A.; Cockell, C. S., Conley, C. A., Dadachova, E.,
Dallas, T. D., de Mey, S., Dong, C., Ellery, A., Ferus, M., Foing, B., Fu,
X., Fujita, K., Lin, Y., Jheeta, S., Hicks, L. J., Hu, S., Kereszturi, A.,
Krassakis, A., Liu, Y., Oberst, J., Michalski, J.,Ranjith, P. M., Rinaldi,
T., Rothery, D., Stavrakakis, H. A., Selbmann, L., Sinha, R. K., Wang, A.,
Williford, K., Vaci, Z., Vago, J. L., Waltemathe, M., and Hallsworth, J. E.:
Mars: new insights and unresolved questions, Int. J. Astrobiol., 20,
394–426, https://doi.org/10.1017/S1473550421000276, 2021.
Cirigliano, A., Tomassetti, M.C., Di Pietro, M., Mura, F., Maneschi, M. L.,
Gentili, M. D., Cardazzo, B., Arrighi, C., Mazzoni, C., Negri, R., and
Rinaldi, T.: Calcite moonmilk of microbial origin in the etruscan Tomba
degli Scudi in Tarquinia, Italy, Sci. Rep., 8, 1–10,
https://doi.org/10.1038/s41598-018-34134-y, 2018.
Cirigliano, A., Mura, F., Cecchini, A., Tomassetti, M. C., Maras, D. F., Di
Paola, M., Meriggi, N., Cavalieri, D., Negri, R., Quagliariello, A.,
Hallsworth, J. E., and Rinaldi, T.: Active microbial ecosystem in Iron-Age
tombs of the Etruscan civilization, Appl. Environ. Microbiol., 23,
3957-3969, https://doi.org/10.1111/1462-2920.15327, 2021a.
Cirigliano, A., Mura, F., Quagliarello, A., Negri, R., and Rinaldi, T.:
Calcium carbonate of microbial origin in the Etruscan tombs of Tarquinia,
1st Italian Space Agency Workshop on Astrobiology. Memorie della Società
Astronomica Italiana/ Journal of the Italian Astronomical Society, Fabrizio
Serra Editore, Pisa-Roma, 92, 64–66, 2021b.
Compère, P., Carnol, M., Barton, H. A., and Rigali, S.: Assessment of the
potential role of Streptomyces in cave moonmilk formation, Front.
Microbiol., 8, 1181, https://doi.org/10.3389/fmicb.2017.01181, 2017.
Cosmidis, J. and Benzerara, K.: Why do microbes make minerals?, C.
R. Géosci., 354, 1–39, https://doi.org/10.5802/crgeos.107, 2022.
Cuadros, J.: Clay minerals interaction with microorganisms: A review, Clay
Miner., 52, 235–261, https://doi.org/10.1180/claymin.2017.052.2.05, 2017.
Dhami, N. K., Reddy, M. S., and Mukherjee, A.: Synergistic role of bacterial
urease and carbonic anhydrase in carbonate mineralization, Biotechnol. Appl.
Bioc., 172, 2552–2561, https://doi.org/10.1007/s12010-013-0694-0, 2014.
Diloreto, Z. A., Garg, S., Bontognali, T. R., and Dittrich, M.: Modern
dolomite formation caused by seasonal cycling of oxygenic phototrophs and
anoxygenic phototrophs in a hypersaline sabkha, Sci. Rep., 11, 4170,
https://doi.org/10.1038/s41598-021-83676-1, 2021.
Dupraz, C., Reid, R. P., Braissant, O., Decho, A. W., Norman, R. S., and
Visscher, P. T.: Processes of carbonate precipitation in modern microbial
mats, Earth-Sci. Rev., 96, 141–162,
https://doi.org/10.1016/j.earscirev.2008.10.005, 2009.
Ehlmann, B. L., Mustard, J. F., Murchie, S. L., Poulet, F., Bishop, J. L.,
Brown, A. J., Calvin, W. M., Clark, R. N., Des Marais, D. J., Milliken, R. E.,
Roach, L. H., Roush, T. L., Swayze, G. A., and Wray, J. J.: Orbital
identification of carbonate-bearing rocks on Mars, Science, 322, 1828–1832,
https://doi.org/10.1126/science.1164759, 2008.
Gonzalez-Pimentel, J. L., Martin-Pozas, T., Jurado, V., Miller, A. Z.,
Caldeira, A. T., Fernandez-Lorenzo, O., Sanchez-Moral, S., and Saiz-Jimenez,
C.: Prokaryotic communities from a lava tube cave in La Palma Island (Spain)
are involved in the biogeochemical cycle of major elements, PeerJ, 9,
e11386, https://doi.org/10.7717/peerj.11386, 2021.
Görgen, S., Benzerara, K., Skouri-Panet, F., Gugger, M., Chauvat, F.,
and Cassier-Chauvat, C.: The diversity of molecular mechanisms of carbonate
biomineralization by bacteria, Discov. Mater., 1, 2,
https://doi.org/10.1007/s43939-020-00001-9, 2021.
Grosch, E. G. and Hazen, R. M.: Microbes, mineral evolution, and the rise of
microcontinents–origin and coevolution of life with early earth,
Astrobiology, 15, 922–939, https://doi.org/10.1089/ast.2015.1302, 2015.
Grottoli, A., Beccaccioli, M., Zoppis, E., Fratini, R. S., Schifano, E.,
Santarelli, M. L., Uccelletti, D., and Reverberi, M.: Nanopore sequencing and
bioinformatics for rapidly identifying cultural heritage spoilage
microorganisms, Front. Mater. Sci. 7, 14,
https://doi.org/10.3389/fmats.2020.00014, 2020.
Grotzinger, J. P. and James, N. P.: Precambrian carbonates: evolution of
understanding, in: Carbonate
Sedimentation and Diagenesis in the Evolving Precambrian World, edited by: Grotzinger, J. P. and James, N. P., Society for
Sedimentary Geology Special Publications, 67, 3–22, ISBN 978-1-56576-072-1, 2000.
Hammes, F. and Verstraete, W.: Key roles of pH and calcium metabolism in
microbial carbonate precipitation, Rev. Environ. Sci.
Bio., 1, 3–7,
https://doi.org/10.1023/A:1015135629155, 2002.
Hartmann, J., Dürr, H. H., Moosdorf, N., Meybeck, M., and Kempe, S.: The
geochemical composition of the terrestrial surface (without soils) and
comparison with the upper continental crust, Int. J. Earth. Sci., 101, 365–376, https://doi.org/10.1007/s00531-010-0635-x, 2012.
Hazen, R. M., Papineau, D., Bleeker, W., Downs, R. T., Ferry, J. M., McCoy,
T. J., Sverjensky, D. A., and Yang, H.: Mineral evolution, Am. Mineral., 93,
1693–1720, https://doi.org/10.2138/am.2008.2955, 2008.
Javaux, E. J.: Challenges in evidencing the earliest traces of life, Nature,
572, 451–460, https://doi.org/10.1038/s41586-019-1436-4, 2019.
Jones, B. and Peng, X.: Abiogenic growth of needle-fiber calcite in spring
towers at Shiqiang, Yunnan Province, China, J. Sediment. Res.,
84, 1021–1040, https://doi.org/10.2110/jsr.2014.82, 2014.
Kaczmarek, S. E., Gregg, J. M., Bish, D. L., Machel, H. G., Fouke, B. W.,
MacNeil, A., Lonnee, J., and Wood, R.: Dolomite, very high-magnesium
calcite, and microbes – Implication for the microbial model of
dolomitization, in: Characterization
and Modeling of Carbonates–Mountjoy Symposium 1, SEPM (Society for
Sedimentary Geology) 109, edited by: Macneil, A. J., Lonnee, J., Wood, R., https://doi.org/10.2110/sepmsp.109.01, 2017.
Kaplan, H. H., Lauretta, D. S., Simon, A. A., Hamilton, V. E., Della Giustina,
D. N., Golish, D. R., Reuter, D. C., Bennett, C. A., Burke, K. N., Campins, H.,
Connolly Jr., H. C., Dworkin, J. P., Emery, J. P., Glavin, D. P., Glotch, T. D.,
Hanna, R., Ishimaru, K., Jawin, E. R., Mccoy, T. J., Porter, N., Sandford,
S. A., Ferrone, S., Clark, B. E., Li, J.-Y., Zou, X.-D., Daly, M. G., Barnouin,
O. S., Seabrook, J. A., and Enos, H. L.: Bright carbonate veins on asteroid
(101955) Bennu: Implications for aqueous alteration history, Science, 370, 676,
https://doi.org /10.1126/science.abc3557, 2020.
Kolesár, M. and Čurlik, J.: Origin, distribution and transformation
of authigenic carbonates in loessic soils, Eur. J. Soil Sci.,
4, 38–43, https://doi.org /10.18393/ejss.50910, 2015.
Kondratyeva, L. M., Shadrina, O. S., Litvinenko, Z. N., and Golubeva, E.
M.: Biogeochemical investigations of the speleothem moonmilk in the karst
Proschalnaya cave (far east, Russia), J. Cave Karst Stud.,
82, 95–105, https://doi.org/10.4311/2019MB0106, 2020.
Lacelle, D., Lauriol, B., and Clark, I. D.: Seasonal isotopic imprint in
moonmilk from Caverne de l'Ours (Quebec, Canada): implications for climatic
reconstruction, Canad. J. Earth Sci., 41, 1411–1423,
https://doi.org/10.1139/e04-080, 2004.
Lee, M. R., Lindgren, P., and Sofe, M. R.: Aragonite, breunnerite, calcite and
dolomite in the CM carbonaceous chondrites: High fidelity recorders of
progressive parent body aqueous alteration, Geochim. Cosmochim. Ac., 144,
126–156, https://doi.org/10.1016/j.gca.2014.08.019, 2014.
Maciejewska, M., Adam, D., Naômé, A., Martinet, L., Tenconi, E., Całusinska,
M., Delfosse, P., Hanikenne, M., Baurain, D., Compère, P., Carnol, M., Barton, H. A., and
and Rigali, S.: Assessment of the Potential Role of Streptomyces in Cave
Moonmilk Formation, Front. Microbiol, 8, 1181,
https://doi.org/10.3389/fmicb.2017.01181, 2017.
Marshall, M.: The water paradox and the origins of life, Nature, 588,
210–213, https://doi.org/10.1038/d41586-020-03461-4, 2020.
Michalski, J. R. and Niles, P. B.: Deep crustal carbonate rocks exposed by
meteor impact on Mars, Nat. Geosci., 3, 751–755,
https://doi.org/10.1038/ngeo971, 2010.
Miller, A. Z., Garcia-Sanchez, A. M., Martin-Sanchez, P. M., Costa Pereira,
M. F., Spangenberg, J. E., Jurado, V., Dionísio, A., Afonso, M. J.,
Iglé sias Chaminé, H. I., Hermosin, B., and Saiz-Jimenez, C.: Origin
of abundant moonmilk deposits in a subsurface granitic environment,
Sedimentology, 65, 1482–1503, https://doi.org/10.1111/sed.12431, 2018.
Miller, A. Z., García-Sánchez, A. M., Coutinho, M. L., Costa Pereira,
M. F., Gázquez, F., Calaforra, J. M., Forti, P., Martínez-Frías,
J., Toulkeridis, T., Caldeira, A. T., and Saiz-Jimenez, C.: Colored microbial
coatings in show caves from the Galapagos Islands (Ecuador): first
microbiological approach, Coatings, 10, 1134,
https://doi.org/10.3390/coatings10111134, 2020.
Millière, L., Gussone, N., Moritz, T., Bindschedler, S., and
Verrecchia, E. P.: Origin of strontium and calcium in pedogenic needle fibre
calcite (NFC), Chem. Geol., 524, 329–344,
https://doi.org/10.1016/j.chemgeo.2019.06.022, 2019.
Morris, R. V., Ruff, S. W., Gellert, R., Ming, D. W., Arvidson, R. E., Clark,
B. C., Golden, D. C., Siebach, K., Klingelhöfer, G., Schröder, C.,
Fleischer, I., Yen, A. S., and Squyres, S. W.: Identification of
carbonate-rich outcrops on Mars by the Spirit rover, Science, 329,
1189667, https://doi.org/10.1126/science.118966, 2010.
Mura, F., Cirigliano, A., Bracciale, M. P., and Rinaldi, T.: Characterization
of Nanostructured Calcium Carbonate found in two ancient Etruscan tombs, AIP
Conf. Proc., 2257, 020011, https://doi.org/10.1063/5.0023677, 2020.
Mura, F., Cirigliano, A., Maras, D., and Rinaldi, T.: Analysis of moonmilk
nanofibers in the etruscan tombs of Tarquinia, AIP Conf.
Proc., 2416, 020014, https://doi.org/10.1063/5.0068804, 2021.
National Center for Biotechnology Information (NCBI): Biogenic calcium carbonate as evidence for life, https://www.ncbi.nlm.nih.gov/bioproject/PRJNA1022455, last access: 29 September 2023.
Nigro, L., Mura, F., Toti, M. P., Cirigliano, A., and Rinaldi, T.: Carbonatogenic
bacteria on the “Motya Charioteer” sculpture, J. Cult. Herit.,
57, 256–264, https://doi.org/10.1016/j.culher.2022.09.009,
2022.
Omoregie, A. I., Palombo, E. A., and Nissom, P. M.: Bioprecipitation of
calcium carbonate mediated by ureolysis: A review, Environ. Eng.
Res., 26, 200379, https://doi.org/10.4491/eer.2020.379, 2021.
Pilorget, C., Okada, T., Hamm, V., Brunetto, R., Yada, T., Loizeau, D., Riu,
L., Usui, T., Moussi-Soffys, A., Hatakeda, K., Nakato, A., Yogata, K., Abe,
M., Aléon-Toppani, A., Carter, J., Chaigneau, M., Crane, B., Gondet, B.,
Kumagai, K., Langevin, Y., Lantz, C., Le Pivert-Jolivet, T., Lequertier, G.,
Lourit, L., Miyazaki, A., Nishimura, M., Poulet, F., Arakawa, M., Hirata,
N., Kitazato, K., Nakazawa, S., Namiki, N., Saiki, T., Sugita, S.,
Tachibana, S., Tanaka, S., Yoshikawa, M., Tsuda, Y., Watanabe, S., and
Bibring, J. P.: First compositional analysis of Ryugu samples by the
MicrOmega hyperspectral microscope, Nat. Astron., 6, 1–5,
https://doi.org/10.1038/s41550-021-01549-z, 2021.
Pomar, L.: Carbonate systems Regional Geology and Tectonics: Principles of
Geologic Analysis, Elsevier, 1, 235–311,
https://doi.org/10.1016/B978-0-444-64134-2.00013-4, 2020.
Portillo, M. C. and Gonzalez, J. M.: Moonmilk deposits originate from
specific bacterial communities in Altamira Cave (Spain), Microb. Ecol., 61,
182–189, https://doi.org/10.1007/s00248-010-9731-5, 2011.
Riding, R.: Microbialites, Stromatolites, and Thrombolites, in: Encyclopedia of Geobiology, edited by: Reitner, J. and
Thiel, V., Encyclopedia of Earth Sciences
Series, Springer, Dordrecht, 635–654,
https://doi.org/10.1007/978-1-4020-9212-1_196, 2011.
Rodriguez-Navarro, C., Cizer, Ö., Kudłacz, K., Ibañez-Velasco, A.,
Ruiz-Agudo, C., Elert, K., Burgos-Cara, A., and Ruiz-Agudo, E.: The multiple
roles of carbonic anhydrase in calcium carbonate mineralization, Cryst. Eng.
Comm., 21, 7407–7423, https://doi.org/10.1039/C9CE01544B, 2019.
Ruggieri, R. and Trippetta, F.: Petrophysical properties variation of
bitumen-bearing carbonates at increasing temperatures from laboratory to
model, Geophysics, 5, 1SO-Z24, https://doi.org/10.1190/geo2019-0790.1,
2020.
Saladino, R., Botta, L., and Di Mauro, E.: The prevailing catalytic role of
meteorites in formamide prebiotic processes, Life, 8, 6,
https://doi.org/10.3390/life8010006, 2018.
Siesser, W. G. and Rogers, J.: An investigation of the suitability of four
methods used in routine carbonate analysis of marine sediments, Deep-Sea
Res., 16, 135–139, https://doi.org/10.1016/0011-7471(71)90021-0, 1971.
Sumner, D. Y., and Grotzinger, J.P.: Herringbone calcite: petrography and
environmental Significance, J. Sediment. Res., 66, 419–429,
https://doi.org/10.1306/D4268360-2B26-11D7-8648000102C1865D, 1996.
Tomassetti, M. C., Cirigliano, A., Arrighi, C., Negri, R., Mura, F.,
Maneschi, M. L., Gentili, M. D., Stirpe, M., Mazzoni, C. and Rinaldi, T.: A
role for microbial selection in frescoes' deterioration in Tomba degli Scudi
in Tarquinia, Italy. Sci. Rep., 7, 6027,
https://doi.org/10.1038/s41598-017-06169-0, 2017.
Trippetta, F., Ruggieri, R., Brandano, M., and Giorgetti, C.: Petrophysical
properties of heavy oil-bearing carbonate rocks and their implications on
petroleum system evolution: Insights from the Majella Massif, Mar. Petrol.
Geol., 111, 350–362, https://doi.org/10.1016/j.marpetgeo.2019.08.035, 2020.
Veizer, J., Hoefs, J., Ridler, R. H., Jensen, L. S., and Lowe, D. R.:
Geochemistry of Precambrian carbonates: I. Archean hydrothermal systems,
Geochim. Cosmochim. Ac., 53, 845–857,
https://doi.org/10.1016/0016-7037(89)90030-6, 1989.
Voosen, P.: NASA mission set to sample carbon-rich asteroid, Science, 370,
158, https://doi.org/10.1126/science.370.6513.158, 2020.
Wood, D. E., Lu, J., and Langmead, B.: Improved metagenomic analysis with
Kraken 2, Genome. Biol. 20, 257, https://doi.org/10.1186/s13059-019-1891-0,
2019.
Zhu, T. and Dittrich, M.: Carbonate precipitation through microbial
activities in natural environment, and their potential in biotechnology: a
review, Frontiers in bioengineering and biotechnology, 4, 4, https://doi.org/10.3389/fbioe.2016.00004, 2016.
Short summary
The history of Earth is a story of the co-evolution of minerals and microbes. We present the evidence that moonmilk precipitation is driven by microorganisms within the rocks and not only on the rock surfaces. Moreover, the moonmilk produced within the rocks contributes to rock formation. The calcite speleothem moonmilk is the only known carbonate speleothem on Earth with undoubted biogenic origin, thus representing a biosignature of life.
The history of Earth is a story of the co-evolution of minerals and microbes. We present the...
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