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Exoplanet Biosignatures Workshop-Without-Walls Review Papers - Discussion Forum

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19 Apr 2017

2. Exoplanet Biosignatures: Understanding Oxygen as a Biosignature in the Context of Its Environment

  1. NExSS Manager

    Contact: Victoria S. Meadow, vsm *at*
    Summary: In this paper we provide an overview of the end-to-end development of O2 as a biosignature for extrasolar planetary observations.   We describe how, during the coevolution of life with the early Earth’s environment, the interplay of sources and sinks of O2 may have suppressed its accumulation in the atmosphere for several billion years, a false negative for biologically-generated O2.   Meanwhile, recent computer modeling research on potential mechanisms in exoplanet environments that may generate relatively high abundances of atmospheric O2 in the absence of a biosphere illustrate the concept of false positives.   We then describe current knowledge of specific photometric, spectroscopic and time-dependent observations of environmental context that could be made by future observatories to identify O2 as a biosignature, and discriminate it from potential false positives.   O2 was originally believed to be an unambiguous indicator for life, but the recent rich body of interdisciplinary research on the early Earth, and the predictive power of star-planet computer models, illustrate O2 as a model for the importance of environmental context in the being able to recognize and interpret biosignatures.

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  2. Mercedes Lopez-Morales

    Great paper and very nicely written!

    I have a comment on section 4.0 (Observational Requirements): the end of paragraph 3 in that section describes how we will be able to detect biosignatures with a combination of high resolution spectrographs and direct imaging instrumentation on ELTs. This is one way, but it is also possible to do this via high-resolution transmission spectroscopy of transiting planets, using the same high resolution spectrographs. This technique will most likely start doing this science first, since we will get the first good targets from TESS, i.e. they will transit, and at least one high resolution spectrograph is already approved as first light instrument on one of the ELTs (this is G-CLEF on the GMT, see e.g. ). In the future we will be able to feed the light of directly imaged planets into high resolution spectrographs like G-CLEF.

    There is also this paper with detailed calculations on how well high resolution spectrographs on ELTs will be able to do this science: . See tables 2 and 3.

    Thanks for putting this paper together.


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  3. Tanai Cardona

    Hi, this is a very exciting paper! Thank you. I want to comment on section “2.1 Evolution of Oxygenic Photosynthesis” because this is my field of expertise. I think I can make a few points that could perhaps help improve this section… or at least provide some food for thought. I apologize in advance for the long commentary, but it is a subject that I am very passionate about.


    “The light reactions of oxygenic photosynthesis in cyanobacteria, algae, and plants use two linked photosystems: photosystems I (PSI) and II (PSII). This linkage allows for the extraction of an electron from water, which has a very positive redox potential (O2/H2O pair; E0' = + 0.87 V) (see overview in Schwieterman et al., this issue).”

    1) Photosystem II extracts 4 electrons from 2 water molecules.

    2) The linked photosystems are not required to oxidize water. In fact, Photosystem II alone is enough to oxidize water. It is possible to have purified PSII with very high water oxidation activity. Therefore, Photosystem I does not contribute to the oxidation of water. The two photosystems in series are required so that the electrons that have been extracted from water can be then redirected to the electron carriers, ferredoxin and NADP+.


    “This configuration of photosynthetic machinery is very complex, and the evolution of cyanobacteria performing oxygenic photosynthesis was preceded by more primitive anoxygenic phototrophs (e.g., Xiong et al., 2000).”

    This is not quite right...

    An important thing to notice regarding the evolution of oxygenic photosynthesis is that all of its complexity evolved after the evolution of water oxidation. The photosynthetic machinery of cyanobacteria appears very complex, especially Photosystem II, but this complexity evolved to enhance the efficiency of water oxidation and to put in place photoprotective, repair, and quality control mechanisms against the formation of singlet oxygen and radical oxygen species. Therefore, all of these complexity evolved to support water oxidation. In other words, it was the evolution of water oxidation to oxygen that triggered the emergence of complexity in the photosynthetic machinery.

    Complexity or simplicity is not a valid argument to establish what is more “primitive” or what comes first. When speaking about evolution, using words like “primitive” should be avoided at all times, because more often than not it turns out to be misleading.

    The authors may be surprised to know then that even though Photosystem II appears fascinatingly complex and sophisticated, in reality it retains many characteristics that can be traced back to the most ancestral form of photochemical reaction centers at the very dawn of photosynthesis. In contrast, certain characteristics of anoxygenic phototrophs that seem primitive are actyally recent evolutionary innovations. I have reviewed and discussed this in great detail in several of my publications (Cardona 2015, Cardona 2016, Cardona 2017).

    I know this may sound a bit unorthodox, but the evolution of reaction center proteins actually suggests that the photosystems employed in oxygenic photosynthesis evolved in parallel to those found in anoxygenic phototrophs, starting from a common origin. This conclusion is well supported by structural and functional comparisons of reaction center proteins, and it is of course reflected in the phylogeny of the reaction center proteins, as I reviewed in Cardona 2015, but see also (Cardona 2016).

    While it may be easy to assume that such "common origin" in the evolution of reaction center proteins was likely anoxygenic, there is no proof against the possibility that such "common origin" was actually oxygenic.

    The cited reference Xiong et al., 2000, while it was at the frontier of our knowledge back then, it is today a bit outdated. Their phylogenetic trees have been revised since (Bryant et al. 2012, Sousa et al. 2013), and several of their conclusions do not stand today.

    I suggest you to cite my review in Photosynthesis Research, 2015, but if you want a higher-profile review on the evolution of photosynthesis, I suggest Blankenship and Hohmann-Marriott (2011), doi: 10.1146/annurev-arplant-042110-103811.

    Perhaps you may want to mention at the beginning of this section that the evolution of oxygenic photosynthesis happened when an ancestral photochemical reaction center evolved the capacity to oxidize water. Perhaps you should say that water oxidation occurs at the Mn4CaO5 cluster, the oxygen evolving complex, coordinated by the core subunits of Photosystem II, and perhaps cite the crystal structure of Photosystem II (Umena et al. 2011).


    Quoting: “One school of thought on the evolutionary transition from anoxygenic to oxygenic photosynthesis emphasizes the importance of the redox potential of electron donors or reductants…” Several publications by Olson and Pierson are cited.

    The considerations by Olson and Pierson are quite sensible, and at first sight make a lot of sense. However, they are mostly speculative and outdated in a number of ways. One assumption they made for example is that Type I reaction centers predate Type II reaction centers. This is a very popular idea that is not supported by phylogenetic analysis and structural/functional comparisons of photochemical reaction centers.

    What we know for sure is that all reaction centers have a common origin and that one of the earliest stages in the evolution of photosynthesis is the event that led to the divergence of Type I and Type II reaction centers. But there is no proof that the most ancestral reaction center of all was one type or the other.

    The considerations on the availability of electron donors, their redox potentials, or the necessity for intermediary electron donors before water are probably not so important when it comes to the origin of water oxidation catalysis. This is because none of the anoxygenic reaction centers directly oxidizes the electron donors. Hydrogen is oxidized by hydrogenases, and light is not needed for the oxidation of hydrogen. Hydrogen sulfide is oxidized by sulfide:quinone oxidoreductase, and light is not needed to drive this reaction. As well, neither iron nor arsenic are oxidized by reaction centers directly and therefore it is unlikely that the availability of these donors or their redox potentials had a strong selective pressure on the evolution of early photochemical reaction centers or water oxidation.

    Unlike H2, H2S, Fe, or As, water is the substrate of a photochemical reaction center, in this case of Photosystem II, and it is only and directly oxidized by Photosystem II. Consider the following:

    As the authors mentioned, there are two types of reaction centers, Type I and Type II. Cyanobacteria are unique because they have both types: a Type II reaction center known as Photosystem II and a Type I reaction center, known as Photosystem I.

    What is perhaps less known is that Photosystem II is not just a Type II reaction center.

    Photosystem II is itself a chimera of Type I and Type II reaction centers. The core subunits of PSII, D1 and D2, originated from a Type II reaction center protein. The antenna proteins of PSII, CP43 and CP47, originated from a Type I reaction center protein. The Mn4CaO5 cluster, where the oxidation of water to oxygen occurs, is coordinated by D1 and CP43. The evolutionary significance of this is not widely understood yet, but it means that the close cooperation of an ancestral Type I and Type II reaction center was required for the evolution of the water oxidizing cluster. The sequence traits and the position of certain cofactors coordinated by D1 and CP43 make it so that the interaction between the ancestral Type I and Type II reaction centers must have been continuous since the origin of photosynthesis (Cardona 2017). While this might sound like speculation, and I fear sounding "unscientific" :) it is acutally rather unequivocal.

    Now, consider this:

    1) There are no known anoxygenic phototrophs with both types of anoxygenic reaction centers

    2) Two photosystems linked in series are required for oxygenic photosynthesis, Photosystem I and II.

    3) Photosystem II is itself a chimera of Type I and Type II reaction centers and both parts contribute to the coordination of the water oxidizing complex.

    It starts to look suspiciously like the evolution of two distinct types of reaction centers was driven by the origin of water oxidation catalysis. I would dare to say that it is in the light of the evolution of water oxidation catalysis that the emergence of photosynthesis on Earth actually makes sense. This perhaps is a bit of a radical position.

    Perhaps, from a more conservative perspective, the most sensible intermediary electron donor before the oxidation of water, was Mn2+, not Fe2+. Mn2+ donating electrons directly to photo-generated tyrosine radicals within an ancestral homodimeric reaction center, as discussed in Cardona et al. (2015), page 1322, third paragraph. However, it is not unreasonable to think that the oxidation of Mn2+ by an ancestral photosystem resulted in the partial or inefficient oxidation of water from the get go (Armstrong 2008).


    The authors state: “it is of course difficult to estimate the likelihood that oxygenic photosynthesis would evolve on an exoplanet.”

    I have a feeling that the authors are biased towards thinking that oxygenic photosynthesis may be very difficult to evolve. The point that I want to make is that the key evolutionary innovation required for the biogenic production of oxygen is the emergence of water oxidation chemistry. To evolve water oxidation chemistry on earth, three things were needed: tetrapyrroles (to make chlorophylls), a protein backbone (to bind the tetrapyrroles), and manganese. All of these were already available to the last universal ancestor of all cellular life.

    For example, it was recently suggested that the last universal common ancestor was capable of nitrogen fixation and methanogenesis (Weiss et al. 2016). Methanogenesis uses Ni-tetrapyrroles built with enzymes homologs to those required for Mg-tetrapyrroles in the synthesis of chlorophyll and bacteriochlorophyll. These enzymes are also homologs to nitrogenases, which have a complex MoFeS cofactor that requires and specialized machinery to be assembled. I guess the authors might be surprised to know that the Mn4CaO5 cluster of Photosystem II is self-assembled, a process known as photoactivation. There is no requirement of a complex biogenesis machinery to make the water-oxidizing complex, it can assembled itself provided that there is light, aqueous Mn2+ and Ca2+.

    I am not saying that water oxidation evolved in the last universal common ancestor, however my most recent work does imply that water oxidation might have arisen soon after the origin of the earliest forms of photoautrophy prior to the events that led to the diversification of the major groups of bacteria (Cardona et al. 2017), some time in the early Archaean.

    In conclusion, I would say that the likelihood of water oxidation chemistry evolving in an exoplanet is at least as likely as the emergence of life itself, or as likely as the evolution of any other biochemical reaction.



    Armstrong, F. A. (2008). "Why did nature choose manganese to make oxygen?" Philosophical Transactions of the Royal Society B-Biological Sciences 363(1494): 1263-1270.

    Bryant, D., Z. Liu, T. LI, F. Zhao, C. G. Klatt, D. Ward, N. U. Frigaard and J. Overmann (2012). Comparative and functional genomics of anoxygenic green bacteria from the taxa Chlorobi, Chloroflexi, and Acidobacteria. Functional Genomics and Evolution of Photosynthetic Systems. R. L. Burnap and W. Vermaas. Dordrecht Springer. 33: 47-102.

    Cardona, T. (2015). "A fresh look at the evolution and diversification of photochemical reaction centers." Photosynthesis Research 126(1): 111-134.

    Cardona, T. (2016). "Reconstructing the origin of oxygenic photosynthesis: Do assembly and photoactivation recapitulate evolution?" Frontiers in Plant Science 7: 257. doi: 10.3389/fpls.2016.00257

    Cardona, T. (2017). "Photosystem II is a chimera of reaction centers." Journal of Molecular Evolution 84(2-3): 149-151.

    Cardona, T., J. W. Murray and A. W. Rutherford (2015). "Origin and evolution of water oxidation before the last common ancestor of the cyanobacteria." Molecular Biology and Evolution 32(5): 1310-1328.

    Cardona, T., P. Sanchez-Baracaldo, A. W. Rutherford and A. W. D. Larkum (2017). "Molecular evidence for the early evolution of photosynthetic water oxidation." BioRxiv 109447. doi:

    Sousa, F. L., L. Shavit-Grievink, J. F. Allen and W. F. Martin (2013). "Chlorophyll biosynthesis gene evolution indicates photosystem gene duplication, not photosystem merger, at the origin of oxygenic photosynthesis." Genome Biology and Evolution 5(1): 200-216.

    Umena, Y., K. Kawakami, J. R. Shen and N. Kamiya (2011). "Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 A." Nature 473(7345): 55-60.

    Weiss, M. C., F. L. Sousa, N. Mrnjavac, S. Neukirchen, M. Roettger, S. Nelson-Sathi and W. F. Martin (2016). "The physiology and habitat of the last universal common ancestor." Nature Microbiology 1(9): 16116. doi: 10.1038/nmicrobiol.2016.116

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  4. Shawn D Domagal-Goldman


    Thanks for that feedback - we certainly want to make sure we adequately capture the capabilities of transit spectroscopy from both the ground and from space.

    Do you mind also looking at the fifth manuscript? That's where we've really focused on the future lineup of observatories.

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  5. Mercedes Lopez-Morales

    OK, will do and send comments by Friday. M. On Wed, Jun 7, 2017 at 10:41 AM, Shawn D Domagal-Goldman @ nexss < This email address is being protected from spambots. You need JavaScript enabled to view it.> wrote: ---- Emailed forum response from This email address is being protected from spambots. You need JavaScript enabled to view it.

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  6. Mercedes Lopez-Morales

    Hi Shawn, I just realized I had already read Yuka's paper and sent comments. Thanks for pointing this out. Mercedes On Wed, Jun 7, 2017 at 10:41 AM, Shawn D Domagal-Goldman @ nexss < This email address is being protected from spambots. You need JavaScript enabled to view it.> wrote: ---- Emailed forum response from This email address is being protected from spambots. You need JavaScript enabled to view it.

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  7. Nancy Kiang

    Tanai - Great points!  I'll defer to the authors on the scope of this paper (it's more about planetary-scale oxygen as a biosignature, while the origins stuff is brief background), but a lot of your points can go into some of the other review papers in this series.

    Re only one photosystem, PSII, being involved in water oxidation, whereas PSI is further down the electron transport chain, YES, let's drive this point home to the astrobiology community.  This is actually covered in the Schwieterman et al. paper on the state of the science, so please look there.  That said, all oxygenic phototrophs still need the two photosystems in series to achieve the "oxygenic" and the "photosynthesis" tasks.  But that topic is big, so we can certainly beef up the literature list of the various issues.

    Re the origins of the reaction centers and of the Mn4CaO5 oxygen evolving complex (OEC), please see the Walker et al. paper on Future Directions. The fine details you elaborate on are beyond the scope of these review papers, but we can include more citations for readers to go to for the details.  Obviously, there are competing theories, including yours, and the origins are not settled, so in the Walker et al. paper, we want to make sure we at least provide a good literature list.  Thanks for all the refs!

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