UvA-DARE (Digital Academic Repository) Stromatolites as Biosignatures of Atmospheric Oxygenation Carbonate Biomineralization and UV-C Resilience in a Geitlerinema sp. - Dominated Culture Popall, R.M.; Bolhuis, H.; Muyzer, G.; Sánchez-Román, M. DOI 10.3389/fmicb.2020.00948 Publication date 2020 Document Version Final published version Published in Frontiers in Microbiology License CC BY Link to publication Citation for published version (APA): Popall, R. M., Bolhuis, H., Muyzer, G., & Sánchez-Román, M. (2020). Stromatolites as Biosignatures of Atmospheric Oxygenation: Carbonate Biomineralization and UV-C Resilience in a Geitlerinema sp. - Dominated Culture. Frontiers in Microbiology, 11, [948]. https://doi.org/10.3389/fmicb.2020.00948 General rights It is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), other than for strictly personal, individual use, unless the work is under an open content license (like Creative Commons). Disclaimer/Complaints regulations If you believe that digital publication of certain material infringes any of your rights or (privacy) interests, please let the Library know, stating your reasons. In case of a legitimate complaint, the Library will make the material inaccessible and/or remove it from the website. Please Ask the Library: https://uba.uva.nl/en/contact, or a letter to: Library of the University of Amsterdam, Secretariat, Singel 425, 1012 WP Amsterdam, The Netherlands. You will be contacted as soon as possible. UvA-DARE is a service provided by the library of the University of Amsterdam (https://dare.uva.nl) Download date:05 Oct 2021 fmicb-11-00948 May 15, 2020 Time: 16:54 # 1 ORIGINAL RESEARCH published: 19 May 2020 doi: 10.3389/fmicb.2020.00948 Stromatolites as Biosignatures of Atmospheric Oxygenation: Carbonate Biomineralization and UV-C Resilience in a Geitlerinema sp. - Dominated Culture Rabja M. Popall1, Henk Bolhuis2, Gerard Muyzer3 and Mónica Sánchez-Román1* Edited by: Akihiko Yamagishi, 1 Earth Sciences Department, Faculty of Science, Vrije Universiteit, Amsterdam, Netherlands, 2 Marine Microbiology & Tokyo University of Pharmacy and Life Biogeochemistry Department, Royal Netherlands Institute for Sea Research, Utrecht University, Den Hoorn, Netherlands, Sciences, Japan 3 Microbial Systems Ecology, Department of Freshwater and Marine Ecology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, Netherlands Reviewed by: Victoria Alexis Petryshyn, University of Southern California, Modern stromatolites are key to the record of past microbial activity preserved in fossil United States Crisogono Vasconcelos, carbonate deposits. Mono-phototrophic cultures dominated by the cyanobacterium ETH Zürich, Switzerland Geitlerinema sp. were obtained from a laboratory-maintained, low magnesium-calcite Emmanuelle Gérard, stromatolite originating from Lagoa Vermelha, Brazil. This lagoonal system has been UMR7154 Institut de Physique du Globe de Paris (IPGP), France described as a Precambrian analog, illustrating a period of photosynthetically induced Fumito Shiraishi, atmospheric oxygenation, which created a global sanctuary from shortwave solar Hiroshima University, Japan radiation and enabled the evolution of modern life on Earth. The enrichment cultures *Correspondence: Mónica Sánchez-Román precipitate carbonates in minimal media, suggesting that cyanobacterial photosynthesis [email protected]; and extracellular polymeric substance production may be crucial in the mineralization of [email protected] the studied stromatolite. We further show that Geitlerinema sp. can build and maintain Specialty section: filamentous mats under long-term UV-C exposure. Our results suggest that present This article was submitted to day stromatolites dominated by cyanobacteria may be interpreted as biosignatures of Microbiological Chemistry atmospheric oxygenation and have implications for the search for putative biological and Geomicrobiology, a section of the journal traces on Mars. Frontiers in Microbiology Keywords: cyanobacteria, biomineralization, UV radiation, stromatolite, microbial carbonate, microbial mats, Received: 21 October 2019 Geitlerinema sp., biosignatures Accepted: 21 April 2020 Published: 19 May 2020 Citation: INTRODUCTION Popall RM, Bolhuis H, Muyzer G and Sánchez-Román M (2020) Stromatolites are the oldest known fossil records of life on Earth. The organo-sedimentary Stromatolites as Biosignatures structures are formed by complex interactions between microbial mat communities and their of Atmospheric Oxygenation: geochemical environment, thus providing insight into the ecosystem at the time of their genesis Carbonate Biomineralization and UV-C Resilience in a Geitlerinema to approximately 3.5 Ga ago in the early Archean (Vasconcelos and McKenzie, 2009; Vasconcelos sp. - Dominated Culture. et al., 2014). Stromatolite abundance peaked in the Proterozoic and strongly decreased toward Front. Microbiol. 11:948. the Cambrian. This decline is attributed to the occurrence of metazoan grazers that started to doi: 10.3389/fmicb.2020.00948 put trophic pressure on microbial mats (Awramik, 1971). Next to predation, a decrease in sea Frontiers in Microbiology| www.frontiersin.org 1 May 2020| Volume 11| Article 948 fmicb-11-00948 May 15, 2020 Time: 16:54 # 2 Popall et al. Stromatolites as Atmospheric Oxygenation Biosignatures water carbonate saturation as well as increasingly complex nucleation sites further reducing kinetic barriers (Kamennaya ecosystems with niche diversification and eukaryotic competition et al., 2012). An ideal matrix for crystal nucleation are the are considered to have impacted stromatolite abundance after amphiphilic EPS, which feature a high uronic acid content and the Mesoproterozoic (Monty, 1973; Grotzinger, 1990; Riding, are suitable for binding both Mg/Ca cations and carbonate 2006). The rare modern stromatolites feature active microbial anions (Decho and Kawaguchi, 2003; Dittrich and Sibler, 2010). mat communities forming lithified discrete buildups, and can Top-layer cyanobacteria are not only photosynthetically active, only be found in few natural environments (Foster et al., 2009; but also the primary EPS producers of the system (Decho and Suosaari et al., 2016). Those habitats are often characterized Kawaguchi, 2003). This renders them key players contributing by an elevated salinity sheltering biofilms from animal grazing majorly to carbonate deposition in modern lithifying mats. and continuous sediment disturbance (Douglas and Beveridge, Molecular traces in the lithified stratum of previously 1998; Schieber, 2007). In accordance with their shallow aquatic studied stromatolites also confirm a significant contribution environment, most of the extant stromatolites contain calcareous of sulfate reduction to lamina formation (Vasconcelos et al., compounds. They are of great importance to the interpretation 2014). A prominent sulfur cycle, however, was only established of ancient stromatolites and key to their record of past microbial as a result of emerging oxygenic photosynthesis during the activity forming lithified deposits (Decho and Kawaguchi, 2003; Great Oxygenation Event (GOE) (Canfield and Raiswell, 1999). Vasconcelos et al., 2006; Vasconcelos and McKenzie, 2009; While anaerobic photosynthesizers were most likely relevant Kazmierczak´ et al., 2015). for the formation of pre-GOE stromatolites (Bosak et al., The functionally and structurally diversified modern 2007), the massive proliferation of oxygenic cyanobacteria stromatolites feature comprehensive communities in distinct facilitated a tremendous diversification of life and an increasingly layers (Vasconcelos and McKenzie, 2009). Comprising complete oxygenated atmosphere (Shestakov and Karbysheva, 2017). cycles of C, N, and S, microbial mats form a nearly closed During the simultaneous establishment of an atmospheric minimal ecosystem and include the major functional groups of ozone shield, light-dependent cyanobacteria were exposed to oxygenic photosynthetic primary producers (Cyanobacteria), the extremely damaging shortwave spectrum of ultraviolet aerobic heterotrophs, sulfur oxidizers, and anaerobic sulfate (UV) solar radiation (Garcia-Pichel, 1998). Sedimentary reducers along a vertical O2 gradient (Visscher and Stolz, habitats may have additionally aggravated the damaging 2005). By definition, stromatolite growth is promoted “through effect of UV-C due to light-trapping effects, resulting in accretion of laminae by the entrapment of sediment and cyanobacterial mats developing highly effective adaptions by participation of carbonate, under active secretion or such as chemical protectants, DNA repair mechanisms direct influence of microorganisms” (Altermann, 2008). The and phototaxis, a behavioral mechanism preserved in fossil mechanism of trapping and binding sediment particles in stromatolites (Garcia-Pichel, 1998). The role of UV-C the microbial mat is less significant in ancient carbonate resilient cyanobacteria in the evolution of aerobic modern stromatolites due to the lack of detritus from higher life forms life-forms is not only of paleontological interest, but also in the Precambrian complementing carbonate sources of significant to understand a possible existence of life on Mars. micrite and erosion, although some Archean microorganisms The finding of organic carbon on Mars recently sparked secreted envelopes of biopolymers which might be identical a new discussion on potential traces