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

Nolwenn Callac,Henrik Skogby,Magnus Ivarsson,Ernest Chi Fru,Nicole R Posth,Kweku K Y Yamoah,Curt Broman,Jayne E Rattray,Stephanos P Kilias,Ariadne Argyraki,Christoffer Hemmingsson,Alan Wiech,Rienk H Smittenberg

doi:10.1038/s41598-017-13910-2

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.

Highlights

Shallow submarine hydrothermal ecosystems occur in the photic zone at water depths less than 200 m below sea level[1,2]
Irrespective of depth or habitat, quantitative polymerase chain reaction (qPCR) analyses indicate that the Calvin Cycle is the main CO2 fixation pathway mediated by microorganisms in this shallow hydrothermal setting, with the predominance of cbbm genes quantified over aclB genes
The Raman data coupled to principal component analysis (PCA) indicates that the three habitats were distinct in mineralogical and chemical composition (Fig. 2)

Summary

Introduction

Shallow submarine hydrothermal ecosystems occur in the photic zone at water depths less than 200 m below sea level[1,2]. While the rTCA cycle may drive carbon fixation in deep-sea hydrothermal systems rather than the Calvin Cycle[11,12], the same cannot be assumed for shallow submarine settings. Our aim here was to investigate the mode of carbon fixation in the shallow submarine hydrothermal environment of Spathi Bay, Milos Island. We identified and quantified key carbon fixation genes from samples collected in three different habitats in Spathi Bay. Two habitats were capped either by white or brown deposits and one was a deposit-free sand reference (Fig. 1a–d). Areas in the direct vicinity of the white (amorphous silica and sulphur-rich) and brown (manganese and iron oxide-rich) deposits have a lower abundance of genes involved in carbon fixation relative to the reference sediment. While CO2 consumption in the sediment is driven by both the hydrothermal CO2 gradient and microbial C-fixation, lipid biomarker analysis further revealed the influence of both plant and microbially derived organic matter in the sediments

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Discussion

Conclusion