The rise of oxygen-driven arsenic cycling at ca. 2.48 Ga

Fru, Ernest Chi; Somogyì, Á.; Albani, Abderrazzak El; Medjoubi, Kadda; Aubineau, Jérémie; Robbins, Leslie J.; Lalonde, Stefan V.; Konhauser, Kurt O.

doi:10.1130/g45676.1

Cited by 31 publications

(26 citation statements)

References 38 publications

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“…2). This is consistent with recent analysis on marine shales, suggesting that arsenate began to accumulate in the ocean only after the Archean eon (10), and compatible with the causal role of the GOE in altering the arsenic chemistry on Earth's surface and driving the genetic expansion of arsenic resistance system.…”

Section: Discussionsupporting

confidence: 91%

“…4). Our results are consistent with geochemical models that predict the predominance of reduced arsenic compounds in the anoxic Archean biosphere (2,3,6,10). Formation of traces of arsenate in the Archean, creating a selective pressure before the GOE (6), could have occurred via microbial mediated arsenite oxidation processes such as anoxygenic photosynthesis (5) or nitrate-dependent respiration (23).…”

Section: Discussionsupporting

confidence: 88%

“…Continental weathering of arsenic at this time is negligible under an atmosphere with very low oxygen levels (<<0.001% compared with present atmospheric level) (9). The rise of atmospheric oxygen (∼1% of present atmospheric levels) during the GOE between 2.4 and 2.3 Bya most likely led to intense oxidative weathering of arsenic-bearing minerals that liberated continental arsenic, predominantly as arsenate, for delivery to oceans from rivers (3,10). These processes would have resulted in the widespread appearance of oxidized arsenic species in the environment.…”

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confidence: 93%

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The Great Oxidation Event expanded the genetic repertoire of arsenic metabolism and cycling

Chen

Sun

Yan

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

114

103

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The rise of oxygen on the early Earth about 2.4 billion years ago reorganized the redox cycle of harmful metal(loids), including that of arsenic, which doubtlessly imposed substantial barriers to the physiology and diversification of life. Evaluating the adaptive biological responses to these environmental challenges is inherently difficult because of the paucity of fossil records. Here we applied molecular clock analyses to 13 gene families participating in principal pathways of arsenic resistance and cycling, to explore the nature of early arsenic biogeocycles and decipher feedbacks associated with planetary oxygenation. Our results reveal the advent of nascent arsenic resistance systems under the anoxic environment predating the Great Oxidation Event (GOE), with the primary function of detoxifying reduced arsenic compounds that were abundant in Archean environments. To cope with the increased toxicity of oxidized arsenic species that occurred as oxygen built up in Earth’s atmosphere, we found that parts of preexisting detoxification systems for trivalent arsenicals were merged with newly emerged pathways that originated via convergent evolution. Further expansion of arsenic resistance systems was made feasible by incorporation of oxygen-dependent enzymatic pathways into the detoxification network. These genetic innovations, together with adaptive responses to other redox-sensitive metals, provided organisms with novel mechanisms for adaption to changes in global biogeocycles that emerged as a consequence of the GOE.

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Section: Discussionsupporting

confidence: 91%

Section: Discussionsupporting

confidence: 88%

mentioning

confidence: 93%

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The Great Oxidation Event expanded the genetic repertoire of arsenic metabolism and cycling

Chen

Sun

Yan

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

114

103

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“…Studies of shales show a significant increase in As(V) before the rise of atmospheric oxygen 27 . This accumulation of oxidized arsenic suggests biological activity and more arsenic cycling during the late Archean.…”

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confidence: 99%

Modern arsenotrophic microbial mats provide an analogue for life in the anoxic Archean

Visscher

Gallagher

Bouton

et al. 2020

Commun Earth Environ

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The earliest evidence of life captured in lithified microbial mats (microbialites) predates the onset of oxygen production and yet, modern oxygenic mats are often studied as analogs based on their morphological similarity and their sedimentological and biogeochemical context. Despite their structural similarity to fossil microbialites, the presence of oxygen in most modern microbial mats disqualifies them as appropriate models for understanding early Earth conditions. Here we describe the geochemistry, element cycling and lithification potential of microbial mats that thrive under permanently anoxic conditions in arsenic laden, sulfidic waters feeding Laguna La Brava, a hypersaline lake in the Salar de Atacama of northern Chile. We propose that these anoxygenic, arsenosulfidic, phototrophic mats are a link to the Archean because of their distinctive metabolic adaptations to a reducing environment with extreme conditions of high UV, vast temperature fluctuations, and alkaline water inputs from combined meteoric and volcanic origin, reminiscent of early Earth.

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“…Sequence alignment and crystal structure analysis of vanadium haloperoxidases has revealed that amino acids that bind the vanadate cofactor are conserved with a family of acid phosphatases (Hemrika, Renirie, Dekker, Barnett, & Wever, ; Littlechild, Garcia‐Rodriguez, Dalby, & Isupov, ; Wever & Hemrika, ). Recently, it has been shown that an increase in arsenate (

{AsO}_{4}^{3 -} false] false] >

) in marine shales after 2.45 Ga represented the establishment of an oxidative component to the arsenic cycle and the presence of toxic arsenate in seawater (Fru et al, ). A rise in dissolved vanadate after the GOE follows this trend of selective pressures against microbial communities in the form of oxidized elements.…”

Section: Discussionmentioning

confidence: 99%

The evolving redox chemistry and bioavailability of vanadium in deep time

et al. 2020

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The incorporation of metal cofactors into protein active sites and/or active regions expanded the network of microbial metabolism during the Archean eon. The bioavailability of crucial metal cofactors is largely influenced by earth surface redox state, which impacted the timing of metabolic evolution. Vanadium (V) is a unique element in geo–bio‐coevolution due to its complex redox chemistry and specific biological functions. Thus, the extent of microbial V utilization potentially represents an important link between the geo‐ and biospheres in deep time. In this study, we used geochemical modeling and network analysis to investigate the availability and chemical speciation of V in the environment, and the emergence and changing chemistry of V‐containing minerals throughout earth history. The redox state of V shifted from a more reduced V(III) state in Archean aqueous geochemistry and mineralogy to more oxidized V(IV) and V(V) states in the Proterozoic and Phanerozoic. The weathering of vanadium sulfides, vanadium alkali metal minerals, and vanadium alkaline earth metal minerals were potential sources of V to the environment and microbial utilization. Community detection analysis of the expanding V mineral network indicates tectonic and redox influence on the distribution of V mineral‐forming elements. In reducing environments, energetic drivers existed for V to potentially be involved in early nitrogen fixation, while in oxidizing environments vanadate (VO43-false]false]>) could have acted as a metabolic electron acceptor and phosphate mimicking enzyme inhibitor. The coevolving chemical speciation and biological functions of V due to earth's changing surface redox conditions demonstrate the crucial links between the geosphere and biosphere in the evolution of metabolic electron transfer pathways and biogeochemical cycles from the Archean to Phanerozoic.

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The rise of oxygen-driven arsenic cycling at ca. 2.48 Ga

Cited by 31 publications

References 38 publications

The Great Oxidation Event expanded the genetic repertoire of arsenic metabolism and cycling

The Great Oxidation Event expanded the genetic repertoire of arsenic metabolism and cycling

Modern arsenotrophic microbial mats provide an analogue for life in the anoxic Archean

The evolving redox chemistry and bioavailability of vanadium in deep time

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