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Abstract The oldest and most wide-ranging signal of biological activity (biosignature) on our planet is the carbon isotope composition of organic materials preserved in rocks. These biosignatures preserve the long-term evolution of the microorganism-hosted metabolic machinery responsible for producing deviations in the isotopic compositions of inorganic and organic carbon. Despite billions of years of ecosystem turnover, evolutionary innovation, organismic complexification, and geological events, the organic carbon that is a residuum of the global marine biosphere in the rock record tells an essentially static story. The ~25‰ mean deviation between inorganic and organic 13C/12C values has remained remarkably unchanged over >3.5 billion years. The bulk of this record is conventionally attributed to early-evolved, RuBisCO-mediated CO2 fixation that, in extant oxygenic phototrophs, produces comparable isotopic effects and dominates modern primary production. However, billions of years of environmental transition, for example, in the progressive oxygenation of the Earth’s atmosphere, would be expected to have accompanied shifts in the predominant RuBisCO forms as well as enzyme-level adaptive responses in RuBisCO CO2-specificity. These factors would also be expected to result in preserved isotopic signatures deviating from those produced by extant RuBisCO in oxygenic phototrophs. Why does the bulk carbon isotope record not reflect these expected environmental transitions and evolutionary innovations? Here, we discuss this apparent discrepancy and highlight the need for greater quantitative understanding of carbon isotope fractionation behavior in extant metabolic pathways. We propose novel, laboratory-based approaches to reconstructing ancestral states of carbon metabolisms and associated enzymes that can constrain isotopic biosignature production in ancient biological systems. Together, these strategies are crucial for integrating the complementary toolsets of biological and geological sciences and for interpretation of the oldest record of life on Earth.
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Effects of RuBisCO and CO 2 concentration on cyanobacterial growth and carbon isotope fractionation
Abstract Carbon isotope biosignatures preserved in the Precambrian geologic record are primarily interpreted to reflect ancient cyanobacterial carbon fixation catalyzed by Form I RuBisCO enzymes. The average range of isotopic biosignatures generally follows that produced by extant cyanobacteria. However, this observation is difficult to reconcile with several environmental (e.g., temperature, pH, and CO2concentrations), molecular, and physiological factors that likely would have differed during the Precambrian and can produce fractionation variability in contemporary organisms that meets or exceeds that observed in the geologic record. To test a specific range of genetic and environmental factors that may impact ancient carbon isotope biosignatures, we engineered a mutant strain of the model cyanobacteriumSynechococcus elongatusPCC 7942 that overexpresses RuBisCO across varying atmospheric CO2concentrations. We hypothesized that changes in RuBisCO expression would impact the net rates of intracellular CO2fixation versus CO2supply, and thus whole‐cell carbon isotope discrimination. In particular, we investigated the impacts of RuBisCO overexpression under changing CO2concentrations on both carbon isotope biosignatures and cyanobacterial physiology, including cell growth and oxygen evolution rates. We found that an increased pool of active RuBisCO does not significantly affect the13C/12C isotopic discrimination (εp) at all tested CO2concentrations, yielding εpof ≈ 23‰ for both wild‐type and mutant strains at elevated CO2. We therefore suggest that expected variation in cyanobacterial RuBisCO expression patterns should not confound carbon isotope biosignature interpretation. A deeper understanding of environmental, evolutionary, and intracellular factors that impact cyanobacterial physiology and isotope discrimination is crucial for reconciling microbially driven carbon biosignatures with those preserved in the geologic record.
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- PAR ID:
- 10476476
- Publisher / Repository:
- Wiley
- Date Published:
- Journal Name:
- Geobiology
- Volume:
- 21
- Issue:
- 3
- ISSN:
- 1472-4677
- Page Range / eLocation ID:
- 390 to 403
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1111/gbi.12543
