Modes of carbon fixation in an arsenic and CO2-rich shallow hydrothermal ecosystem

Abstract

The seafloor sediments of Spathi Bay, Milos Island, Greece, are part of the largest arsenic-CO2-rich shallow submarine hydrothermal ecosystem on Earth. Here, white and brown deposits cap chemically distinct sediments with varying hydrothermal influence. All sediments contain abundant genes for autotrophic carbon fixation used in the Calvin-Benson-Bassham (CBB) and reverse tricaboxylic acid (rTCA) cycles. Both forms of RuBisCO, together with ATP citrate lyase genes in the rTCA cycle, increase with distance from the active hydrothermal centres and decrease with sediment depth. Clustering of RuBisCO Form II with a highly prevalent Zetaproteobacteria 16S rRNA gene density infers that iron-oxidizing bacteria contribute significantly to the sediment CBB cycle gene content. Three clusters form from different microbial guilds, each one encompassing one gene involved in CO2 fixation, aside from sulfate reduction. Our study suggests that the microbially mediated CBB cycle drives carbon fixation in the Spathi Bay sediments that are characterized by diffuse hydrothermal activity, high CO2, As emissions and chemically reduced fluids. This study highlights the breadth of conditions influencing the biogeochemistry in shallow CO2-rich hydrothermal systems and the importance of coupling highly specific process indicators to elucidate the complexity of carbon cycling in these ecosystems.

Precipitation of Mn Oxides in Quaternary Microbially Induced Sedimentary Structures (MISS), Cape Vani Paleo-Hydrothermal Vent Field, Milos, Greece

“…The MnMISS display bulk and lipid-specific δ 13 Corg signatures, which are comparable to those extracted from the modern day Mn oxide (birnessite) depositing non-cyanobacterial mats (−18% to −20% , and −19.7% to −22.6% , respectively), in shallow-seafloor hydrothermal sediments from Spathi Bay, SSE Milos coast [86]. In addition, the modern mats, are composed entirely of microbial guilds that fix and utilise carbon primarily by the Calvin cycle [86]. Consequently, similarities in δ 13 C org between the modern and past environments suggest primary carbon fixation mainly associated with the Calvin cycle in the MnMISS.…”

“…Sterols, (cholesterol and campesterol), biosynthesised by both plants and algae, were identified in two samples where the most abundant triterpenoid was cholesterol. For comparison Figure 6B shows a modern day active hydrothermal sediment from Spathi Bay, S. Milos [86]. The same major lipid groups and types are seen in Figure 6A,B but an increased number of low molecular weight lipids and triterpenoid lipids, presumably the less recalcitrant fraction, are observed in the modern day sediments.…”

“…Light C org isotope compositions have been used to support a microbial interpretation of putative MISS [96][97][98]. The MnMISS display bulk and lipid-specific δ 13 Corg signatures, which are comparable to those extracted from the modern day Mn oxide (birnessite) depositing non-cyanobacterial mats (−18% to −20% , and −19.7% to −22.6% , respectively), in shallow-seafloor hydrothermal sediments from Spathi Bay, SSE Milos coast [86]. In addition, the modern mats, are composed entirely of microbial guilds that fix and utilise carbon primarily by the Calvin cycle [86].…”

“…The occurrence of long chain alkanes with specific δ 13 C values in the range of −24.3% to −29.0% , together with sterols, strongly suggest an origin from C3 plants. Plant lipids described by Callac et al (2017) [86] in the modern day Spathi Bay hydrothermal sediments ( Figure 6B), where seagrasses enriched their membrane lipids in 13 C by up to a factor of two, relative to the bulk sediment. Also comparable were the FAME values −31.6% to −29.5% reported in brown-capped sediments, in the modern day Spathi bay sediments.…”

Arsenic and high affinity phosphate uptake gene distribution in shallow submarine hydrothermal sediments

“…A number of studies have identified and successfully characterized microbial communities thriving in hydrothermal vent fields impacted by some of the most elevated As concentrations (e.g., Dando et al 1995; Bayraktarov et al 2013; Giovannelli et al 2013; Price et al 2013a, b; Ruiz-Chancho et al 2013; Gilhooly et al 2014; Godelitsas et al 2015; Callac et al 2017). Nonetheless, a mechanistic understanding of how life copes with high As conditions, the chemical and physical processes that regulate dissolved As content, and the potentially biolimiting phosphate concentrations caused by coprecipitation with hydrothermal Fe(III)(oxyhydr)oxides (e.g., Feely et al 1996, 1998; Wheat et al 1996; Schaller et al 2000; Hawkes et al 2014), remain to be clarified for these environments.…”