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Final Report Summary - BIOCTRACK (The bacterial C-isotope archive: Tracking the biogeosphere from past to present)

Summary of project objectives:
Anoxygenic phototrophic bacteria use light energy to oxidize sulfide or iron and fix carbon out of CO2 to build and maintain cell biomass in environments with little to no oxygen (Widdel et al., 1993; Pfennig, 1967). The metabolism these bacteria carry out is considered one of the earliest evolved on Earth (Xiong, 2006) and studies of Precambrian rocks, as well as laboratory and field experiments, provide evidence for this microbial metabolism in ancient aqueous environments (Konhauser et al., 2002; Brocks et al., 2005; Posth et al., 2013; Crowe et al., 2008; Zerkle et al., 2009; Canfield et al., 2010). As with their modern counterparts, ancient anoxygenic phototrophic bacteria inhabited the light-penetrated water column of oxygen-poor seas. Their remains may have been preserved in the sediment which has been altered to sedimentary rock over geological time. The challenge is to find an appropriate tool to link the bacteria in the water column to any remaining traces of their presence in the sediment in order to paint a picture of life on early Earth.
To this end, we combined the tools of isotope geochemistry with the study of modern model lakes of ancient oceans. Different types of anoxygenic phototrophic bacteria (purple sulfur bacteria (PSB) and green sulfur bacteria (GSB)) use different enzymatic pathways for CO2 fixation, and each of these pathways have a specific extent of C-isotope fractionation. We studied the carbon isotopic composition of bacterial biomass in the water column, settling material and sediment of sulfide-rich (Lake Cadagno, Switzerland) and iron-rich (Lake La Cruz, Spain) lakes. We complemented this field research with laboratory experiments. The ultimate goal was to determine whether these combined tools could be used to trace these bacteria in ancient sedimentary environments. In this study, there were three main questions summarized as work packages (WP) below:
WP1: How do anoxygenic phototrophic bacteria fractionate C-isotopes via carbon fixation in the presence of dissolved iron and sulfur, as well as when carbon is in surplus or limited?
WP2: In bacterial communities, is the bulk C-isotope composition in situ determined by a dominant species or is it an integration of all species present?
WP3: Does biomineralization and diagenesis influence the isotopic composition of an aquatic microbial system, and are isotopic signatures preserved?
Work performed since the beginning of the project: C-isotope fractionation (Δ13C) was determined by calculating the difference between the isotopic composition (13C/12C) of the CO2 source (dissolved inorganic carbon, DIC) and the 13C/12C of the microbial biomass (particulate organic carbon, POC). The C-isotope fractionation in the lake chemocline dominated by anoxygenic phototrophic bacteria was compared to that in pure anoxygenic phototroph cultures. The first year of the project focused on sulfur-rich Lake Cadagno, Swiss Alps and the second year of the project focused on iron-rich Lake La Cruz, Cuenca, Spain. Both lakes are stratified, meaning that oxygen-rich surface waters overlay oxygen-poor bottom water. At the light-penetrated chemocline between the water layers, a community of anoxygenic phototrophic bacteria thrives. Bacteria culture experiments were carried out with strains isolated from the lakes. These bacteria have been model organisms since their isolation from the lakes and are, in part, fully characterized and deposited in culture type collections (Peduzzi et al., 2012 for details). In addition, we were invited to join a Swedish team investigating shallow hydrothermal vents off Milos Island, Greece. Using the methods applied in Cadagno and La Cruz, we studied bacterial C-isotope fractionation and its links to iron, carbon and arsenic element cycling.

Main results
1. Anoxygenic sulfide-oxidizing phototrophic bacteria in Lake Cadagno
Light penetrates the Lake Cadagno chemocline, where oxygen-rich top waters meet sulfidic, oxygen-poor bottom waters, supporting a community of anoxygenic phototrophic bacteria (both PSB and GSB) (Tonolla et al., 2017). Recent studies determined the C-isotope fractionation (∆13C) in the sediment (where ∆13C = δ13CDIC - δ13CPOC; Schubert et al., 2011), but ∆13C was never determined in the water column where bacterial populations actively cycle sulfur. Here, we found a high C-isotope fractionation of ∆13C~32‰ in the chemocline. This high fractionation was also detected in sediment traps, which gather settling material, although the size of the fractionation was dampened due to microbial degradation processes (∆13C~31‰). To determine the relative contributions of the main bacterial populations to these high fractionations, we calculated a carbon isotope mass balance using the C-isotope fractionation determined in pure cultures and in the lake. It was found that C-isotope fractionation was driven by anoxygenic phototrophic bacteria and the influence of the PSB and GSB changed over the season. The contribution of PSB and GSB to the C-isotope fractionation could also be traced in the material settling in the water and in the lake sediment. Taken together with supporting data, such as lipid biomarker studies, these results offer a firmer understanding of diagenetic influences on bacterial biomass over long geological timeframes. This work resulted in a book chapter (Tonolla et al., 2017) and a manuscript in review.
2. Anoxygenic Fe(II)-oxidizing phototrophic bacteria and the C-isotope record of Lake La Cruz
Anoxygenic phototrophic bacteria can also oxidize Fe(II), fix CO2 and produce cell-Fe(III) (hydr)oxide aggregates. These biogenic Fe(III) minerals may be important vehicles for carbon transport in the water column, in carbon preservation (Lalonde et al., 2012), and in how biomass and Fe minerals are altered through diagenetic processes (Posth et al., 2014). Lake La Cruz is an iron rich, stratified lake with a population of anoxygenic phototrophs. We sampled the water column, sediment traps and sediment cores in September 2014. In parallel, we tested C-isotope fractionation in cultures of anoxygenic Fe(II)-oxidizing phototrophic bacteria. A larger fractionation was observed in the PSB cultures than in the GSB cultures (∆13C~24‰ for PSB Rhodobacter ferrooxidans sp. SW2; ∆13C~10‰ for GSB Chlorobium ferrooxidans sp. KoFox). Cycling and diagenesis studies with the biogenic Fe(III) minerals formed by these strains showed a ~3-5‰ shift in the C-isotope composition of the organic carbon in the cell-Fe(III) mineral aggregates due to diagenesis. This shift was not observed in similar studies with sulfide-oxidizing photoautotrophs and suggests Fe(III) mineral transformation influences C-isotopic composition of biogenic minerals after diagenesis (Posth et al., 2013; 2014). Further isotopic mass balance calculations, metagenome and mineralogical analysis of Lake La Cruz will help constrain the processes behind this observation. This work resulted in two manuscripts in progress.
3. C-isotope fractionation in Spathi Bay and implications for microbial Fe, As, and C cycling
The shores off of Milos, Greece are shallow and hydrothermally active, representing another potential early Earth scenario. We investigated bacterial photosynthetic CO2 fixation and the As, Fe and C element cycling in the water column, microbial mats, and sediment using isotope analysis and microbial community profiling (6/2014). We found that the hydrothermally active sediments are marked by a low genetic abundance compared to reference sediments not affected by hydrothermal activity. The Spathi shallow submarine hydrothermal vents differ from hydrothermal environments at seafloor spreading centers because in light-penetrated shallow vent environments, photosynthetic as well as chemosynthetic processes play an important role. The quantification of specific genes involved in autotrophic carbon fixation in Spathi Bay indicates that the RuBisCo form II (Calvin cycle) is the predominant CO2 fixation pathway in the arsenic-CO2-rich shallow submarine hydrothermal sediments as supported by the isotopic data. This differs markedly from deep-sea hydrothermal settings in which the reverse tricarboxylic acid cycle (rTCA cycle) appears to be the main route to carbon fixation (Campbell& Cary, 2004; Nakagawa & Takai, 2008). This work resulted in two manuscripts in progress.
Study Impact: Results of BioCTrack will help interpretation of the rock record to understand the nature and evolution of early life on our planet. By extension, we can understand how life and environment continues to evolve in relation to one another on a changing planet. The project public website can be found at: http://www.sdu.dk/om_sdu/institutter_centre/i_biologi/forskning/forskningsprojekter/bioctrack

References cited:
Brocks JJ et al. (2005) Nature, 437, 866-870.
Campbell BJ & Cary SC (2004) Appl Environ Microbiol, 70(10):6282-6289.
Canfield DE et al. (2010) Geology, 38, 415-418.
Crowe SA et al. (2008) Proc Natl Acad Sci USA, 105, 15938-15943.
Konhauser KO et al. (2002) Geology, 30, 1079-1082.
Nakagawa S & Takai K (2008) FEMS Microbiology Ecology, 65(1):1-14.
Pfennig N (1967) Annual Review of Microbiology, 21, 285-324.
Posth NR et al. (2013) Chem. Geol., 362, 66-73.
Posth NR et al. (2014) Earth-Science Reviews, 135, 103-121.
Schubert CJ et al. (2011) FEMS Microbiology Ecology, 76, 26-38.
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Tonolla M et al. (2017) Ecology of Meromictic Lakes. Springer Verlag. Ecological Studies, Vol 228.
Widdel F et al.(1993) Nature, 362, 834-836.
Xiong J. (2006Genome Biology 7(12), 245.1-245.5.
Zerkle AL et al. (2009) Geochimica et Cosmochimica Acta, 73, 291-306.

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Inge Blond Kroun, (Project Coordinator)
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Record Number: 196786 / Last updated on: 2017-04-06
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