Current Biology Vol 25 No 5 R192
Cyanobacterial Evolution: Fresh Insight into Ancient Questions The invention of oxygenic photosynthesis by cyanobacteria 2.4 billion years ago forever transformed Earth. This biogeochemical shift set into motion the evolution of subsequent microbial metabolisms and lifestyles. A new study provides a novel approach in piecing together evidence for how this evolutionary transition may have occurred. Patrick M. Shih Of all the bacterial phyla, the cyanobacteria stand out as a group that is intimately intertwined with the defining geological feature of Earth: the presence of both water and oxygen. Even more amazing is that this planet-changing metabolism has only evolved once: in over three billion years of bacterial evolution, only cyanobacteria have reaped the benefits of stripping electrons from a globally plentiful molecule such as water in order to drive photosynthesis, producing oxygen as a byproduct. Plants and other eukaryotes only gained this ability by commandeering cyanobacterial endosymbionts into plastid organelles. Prior to the metabolic innovation of oxygenic photosynthesis, the world was an anaerobic landscape, dramatically different from the present day. Because of the importance of how cyanobacteria came to become masters of oxygenic photosynthesis, understanding the origins of this biological feat has perplexed scientists from different fields spanning disciplines such as biology, chemistry, geology, and paleontology. A new study by Harel et al. [1] reported in this issue of Current Biology has compiled and analyzed protein similarity networks from an extensive list of bacteria from disparate redox lifestyles to get at the heart of how cyanobacteria evolved and how their predecessors lived. Although cyanobacterial evolution is fundamental to many aspects of our understanding of early life, there is a high level of uncertainty regarding how and when photosynthesis evolved. Traditionally, scientists have relied on the geological and fossil record to study ancient biological events. The geological record has been crucial in providing evidence for which microbial metabolisms were present in Archean sediments [2,3],
providing novel hypotheses as to how photosynthesis arose [4]. However, it is more difficult to pinpoint and prove which specific organisms were responsible for these metabolisms; thus, scientists have also turned to the fossil record. Because all Precambrian life was microbial, assigning taxonomic lineages to microbial fossils is inherently challenging due to the limited number of morphological markers that can be used to identify them unequivocally. This difficulty is highlighted by the controversy surrounding the authenticity of microfossils dating from over three billion years ago as either cyanobacteria or artifacts formed from amorphous graphite [5,6]. Molecular phylogenetics has drastically advanced the field of systematics in clarifying evolutionary relationships that were once impossible to discern; however, interpreting deep evolutionary relationships is still difficult, as there may not be adequate levels of phylogenetic signal to fully reconstruct phylogenetic relationships at the deepest nodes of the Tree of Life [7,8]. In order to address these phylogenetic challenges, scientists have pursued different approaches in improving the phylogenetic signal necessary to more confidently reconstruct ancient relationships, such as improved phylogenetic coverage [9], use of horizontal gene transfer events as phylogenetic information [10], and use of gene duplication events [11–13]. Although no one method is a silver bullet, the culmination of the body of literature devoted to the deep evolutionary placement of cyanobacteria within the Tree of Life has provided many clues, not always in agreement, for hypotheses concerning the origin of this phylum.
With a scant fossil record and molecular phylogenetics methods being strained with such deep evolutionary questions, Harel et al. [1] present an outside-the-box approach complementary to traditional phylogenetic approaches by instead utilizing protein similarity networks to provide clues as to how and from whom cyanobacteria evolved. They examine 48 cyanobacterial and 84 microbial proteomes that represent four major metabolic groups: methanogens, obligate anaerobes, facultative aerobes, and obligate aerobes. Over the course of Earth’s history, the planet has slowly transitioned from highly anoxic to a more oxidizing environment. Thus, one would expect the emergence of each of these groups to come in order from most reducing to most oxidizing. By utilizing protein similarity networks, connections between the different metabolic groups can be represented, providing evidence for which groups are more closely associated with one another. Harel et al. [1] recapitulate the expected order of relation between these metabolic groups, placing cyanobacteria fittingly between anaerobes and obligate aerobes. These findings logically make sense: if cyanobacteria were the first organisms in an anaerobic world to evolve oxygenic photosynthesis, it would be reasonable to suspect that they would have deep connections with both the preexisting anaerobes and the subsequently evolving aerobes. One of the most interesting implications of the study is how metabolic innovation may drive biological diversity. What would life look like had oxygenic photosynthesis never evolved? Aerobic respiration would most likely never have evolved, drastically changing what we know of many branches scattered across the Tree of Life. With evidence connecting cyanobacteria to both anaerobes and aerobes, one can infer that the innovation of oxygenic photosynthesis opened an entirely new metabolic chapter in life’s history. It seems likely that more complex forms of life such as eukaryotes may not have been able to evolve in the absence of respiration. In line with this, a growing body of evidence has suggested that
Dispatch R193
References Obligate aerobes
Oxidizing
Facultative aerobes Cyanobacteria Obligate anaerobes Methanogens
Atmospheric O2 (% of PAL)
Archean
Proterozoic
Reducing
Phanerozoic
100 10 1 0.1 4000
3500
3000
2500
2000
1500
Millions of years ago
1000
500
0 Current Biology
Figure 1. Succession of various microbial metabolic groups. (Upper) The Earth’s environment became more oxidizing due to the evolution of oxygenic photosynthesis in cyanobacteria after the Great Oxidation Event circa 2.4 billion years ago. Subsequently, various aerobes are thought to have evolved. The various redox lifestyles are colored on a scale from reducing to oxidizing metabolisms. Cyanobacteria are highlighted in red as they have deep connections between both anaerobes and aerobes. Dashed lines indicate uncertainty as to the exact timing of the origin of the various metabolic groups. (Lower) Schematic of oxygen levels as a percentage of present atmospheric levels (PAL). The Great Oxidation Event occurred 2.4 billion years ago, whereas a second increase in oxygen levels to current atmospheric concentrations occurred 800 million years ago.
without a second jump in atmospheric oxygen concentration during the late Proterozoic, circa 800 million years ago (Figure 1), animals would never have evolved [14,15]. By showing the placement of cyanobacteria as a hub with connections between anaerobes and aerobes, network analyses provide further evidence for how the rise of oxygenic photosynthesis was the necessary catalyst to kick-start the aerobic revolution that progressed and continued to the present. Perhaps the most ambitious aspect of the study by Harel et al. [1] is their attempt to reconstruct the metabolic capabilities of the cyanobacterial progenitor. In order to grasp the difficulty of the question Harel et al. [1] have set out to answer, an analogy can be drawn from the more common example of birds and dinosaurs. It would be difficult to imagine what the ancient predecessors of birds, i.e. dinosaurs, would look like if we had no access to fossil data and had only ever seen modern crocodiles and birds. It would be a far stretch of the imagination to concoct the wide range of morphological differences that we know to have existed based on the dinosaur fossil record. Now, imagine doing this with an
ancient evolutionary relationship more than an order of magnitude older and microbial. Reconstructing the genomic and metabolic repertoire of ancestral cyanobacteria is no easy task. Impressively, the results extrapolated from the protein similarity networks provide evidence of various functions such as the biosynthesis of photosynthetic pigments, hydrogenase, DNA repair, and many other functions that make sense for a phototroph in the anoxic Archean world. It is important to keep in mind that it is impossible to definitively know the answer to the challenging questions that surround the origin of oxygenic photosynthesis and cyanobacteria. Without a time machine, we will never be able to perform genome sequencing of organisms that existed billions of years ago. In light of this humbling fact, novel studies such as Harel et al. provide keen insight that will continue to fuel the debate around this hotly contested field. Nonetheless, it is studies like this that will also help push the field forward and promote the discussion necessary to prompt scientists to come up with the next creative approach to addressing this incredibly difficult yet profoundly important question.
1. Harel, A., Karkar, S., Cheng, S., Falkowski, P.G., and Bhattacharya, D. (2015). Deciphering primordial cyanobacterial genome functions from protein network analysis. Curr. Biol. 25, 628–634. 2. Rye, R., and Holland, H.D. (1998). Paleosols and the evolution of atmospheric oxygen; a critical review. Am. J. Sci. 298, 621–672. 3. Shen, Y., Buick, R., and Canfield, D.E. (2001). Isotopic evidence for microbial sulphate reduction in the early Archaean era. Nature 410, 77–81. 4. Johnson, J.E., Webb, S.M., Thomas, K., Ono, S., Kirschvink, J.L., and Fischer, W.W. (2013). Manganese-oxidizing photosynthesis before the rise of cyanobacteria. Proc. Natl. Acad. Sci. USA 110, 11238–11243. 5. Schopf, J.W. (1993). Microfossils of the Early Archean Apex chert: new evidence of the antiquity of life. Science 260, 640–646. 6. Brasier, M.D., Green, O.R., Jephcoat, A.P., Kleppe, A.K., Van Kranendonk, M.J., Lindsay, J.F., Steele, A., and Grassineau, N.V. (2002). Questioning the evidence for Earth’s oldest fossils. Nature 416, 76–81. 7. Roger, A.J., and Hug, L.A. (2006). The origin and diversification of eukaryotes: problems with molecular phylogenetics and molecular clock estimation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 1039–1054. 8. Philippe, H., and Forterre, P. (1999). The rooting of the universal Tree of Life is not reliable. J. Mol. Evol. 49, 509–523. 9. Shih, P.M., Wu, D., Latifi, A., Axen, S.D., Fewer, D.P., Talla, E., Calteau, A., Cai, F., Tandeau de Marsac, N., Rippka, R., et al. (2013). Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc. Natl. Acad. Sci. USA 110, 1053–1058. 10. Abby, S.S., Tannier, E., Gouy, M., and Daubin, V. (2012). Lateral gene transfer as a support for the tree of life. Proc. Natl. Acad. Sci. USA 109, 4962–4967. 11. Iwabe, N., Kuma, K., Hasegawa, M., Osawa, S., and Miyata, T. (1989). Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc. Natl. Acad. Sci. USA 86, 9355–9359. 12. Gogarten, J.P., Kibak, H., Dittrich, P., Taiz, L., Bowman, E.J., Bowman, B.J., Manolson, M.F., Poole, R.J., Date, T., and Oshima, T. (1989). Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes. Proc. Natl. Acad. Sci. USA 86, 6661–6665. 13. Shih, P.M., and Matzke, N.J. (2013). Primary endosymbiosis events date to the later Proterozoic with cross-calibrated phylogenetic dating of duplicated ATPase proteins. Proc. Natl. Acad. Sci. USA 110, 12355–12360. 14. Planavsky, N.J., Reinhard, C.T., Wang, X., Thomson, D., McGoldrick, P., Rainbird, R.H., Johnson, T., Fischer, W.W., and Lyons, T.W. (2014). Low Mid-Proterozoic atmospheric oxygen levels and the delayed rise of animals. Science 346, 635–638. 15. Mills, D.B., Ward, L.M., Jones, C., Sweeten, B., Forth, M., Treusch, A.H., and Canfield, D.E. (2014). Oxygen requirements of the earliest animals. Proc. Natl. Acad. Sci. USA 111, 4168–4172.
Joint BioEnergy Institute, 5885 Hollis St, Emeryville, CA 94608, USA and Physical Biosciences Division, Lawrence Berkeley National Laboratory, One Cyclotron Rd, Berkeley, CA 94720, USA. E-mail: [email protected]
http://dx.doi.org/10.1016/j.cub.2014.12.046
Cyanobacterial Evolution: Fresh Insight into Ancient Questions The invention of oxygenic photosynthesis by cyanobacteria 2.4 billion years ago forever transformed Earth. This biogeochemical shift set into motion the evolution of subsequent microbial metabolisms and lifestyles. A new study provides a novel approach in piecing together evidence for how this evolutionary transition may have occurred. Patrick M. Shih Of all the bacterial phyla, the cyanobacteria stand out as a group that is intimately intertwined with the defining geological feature of Earth: the presence of both water and oxygen. Even more amazing is that this planet-changing metabolism has only evolved once: in over three billion years of bacterial evolution, only cyanobacteria have reaped the benefits of stripping electrons from a globally plentiful molecule such as water in order to drive photosynthesis, producing oxygen as a byproduct. Plants and other eukaryotes only gained this ability by commandeering cyanobacterial endosymbionts into plastid organelles. Prior to the metabolic innovation of oxygenic photosynthesis, the world was an anaerobic landscape, dramatically different from the present day. Because of the importance of how cyanobacteria came to become masters of oxygenic photosynthesis, understanding the origins of this biological feat has perplexed scientists from different fields spanning disciplines such as biology, chemistry, geology, and paleontology. A new study by Harel et al. [1] reported in this issue of Current Biology has compiled and analyzed protein similarity networks from an extensive list of bacteria from disparate redox lifestyles to get at the heart of how cyanobacteria evolved and how their predecessors lived. Although cyanobacterial evolution is fundamental to many aspects of our understanding of early life, there is a high level of uncertainty regarding how and when photosynthesis evolved. Traditionally, scientists have relied on the geological and fossil record to study ancient biological events. The geological record has been crucial in providing evidence for which microbial metabolisms were present in Archean sediments [2,3],
providing novel hypotheses as to how photosynthesis arose [4]. However, it is more difficult to pinpoint and prove which specific organisms were responsible for these metabolisms; thus, scientists have also turned to the fossil record. Because all Precambrian life was microbial, assigning taxonomic lineages to microbial fossils is inherently challenging due to the limited number of morphological markers that can be used to identify them unequivocally. This difficulty is highlighted by the controversy surrounding the authenticity of microfossils dating from over three billion years ago as either cyanobacteria or artifacts formed from amorphous graphite [5,6]. Molecular phylogenetics has drastically advanced the field of systematics in clarifying evolutionary relationships that were once impossible to discern; however, interpreting deep evolutionary relationships is still difficult, as there may not be adequate levels of phylogenetic signal to fully reconstruct phylogenetic relationships at the deepest nodes of the Tree of Life [7,8]. In order to address these phylogenetic challenges, scientists have pursued different approaches in improving the phylogenetic signal necessary to more confidently reconstruct ancient relationships, such as improved phylogenetic coverage [9], use of horizontal gene transfer events as phylogenetic information [10], and use of gene duplication events [11–13]. Although no one method is a silver bullet, the culmination of the body of literature devoted to the deep evolutionary placement of cyanobacteria within the Tree of Life has provided many clues, not always in agreement, for hypotheses concerning the origin of this phylum.
With a scant fossil record and molecular phylogenetics methods being strained with such deep evolutionary questions, Harel et al. [1] present an outside-the-box approach complementary to traditional phylogenetic approaches by instead utilizing protein similarity networks to provide clues as to how and from whom cyanobacteria evolved. They examine 48 cyanobacterial and 84 microbial proteomes that represent four major metabolic groups: methanogens, obligate anaerobes, facultative aerobes, and obligate aerobes. Over the course of Earth’s history, the planet has slowly transitioned from highly anoxic to a more oxidizing environment. Thus, one would expect the emergence of each of these groups to come in order from most reducing to most oxidizing. By utilizing protein similarity networks, connections between the different metabolic groups can be represented, providing evidence for which groups are more closely associated with one another. Harel et al. [1] recapitulate the expected order of relation between these metabolic groups, placing cyanobacteria fittingly between anaerobes and obligate aerobes. These findings logically make sense: if cyanobacteria were the first organisms in an anaerobic world to evolve oxygenic photosynthesis, it would be reasonable to suspect that they would have deep connections with both the preexisting anaerobes and the subsequently evolving aerobes. One of the most interesting implications of the study is how metabolic innovation may drive biological diversity. What would life look like had oxygenic photosynthesis never evolved? Aerobic respiration would most likely never have evolved, drastically changing what we know of many branches scattered across the Tree of Life. With evidence connecting cyanobacteria to both anaerobes and aerobes, one can infer that the innovation of oxygenic photosynthesis opened an entirely new metabolic chapter in life’s history. It seems likely that more complex forms of life such as eukaryotes may not have been able to evolve in the absence of respiration. In line with this, a growing body of evidence has suggested that
Dispatch R193
References Obligate aerobes
Oxidizing
Facultative aerobes Cyanobacteria Obligate anaerobes Methanogens
Atmospheric O2 (% of PAL)
Archean
Proterozoic
Reducing
Phanerozoic
100 10 1 0.1 4000
3500
3000
2500
2000
1500
Millions of years ago
1000
500
0 Current Biology
Figure 1. Succession of various microbial metabolic groups. (Upper) The Earth’s environment became more oxidizing due to the evolution of oxygenic photosynthesis in cyanobacteria after the Great Oxidation Event circa 2.4 billion years ago. Subsequently, various aerobes are thought to have evolved. The various redox lifestyles are colored on a scale from reducing to oxidizing metabolisms. Cyanobacteria are highlighted in red as they have deep connections between both anaerobes and aerobes. Dashed lines indicate uncertainty as to the exact timing of the origin of the various metabolic groups. (Lower) Schematic of oxygen levels as a percentage of present atmospheric levels (PAL). The Great Oxidation Event occurred 2.4 billion years ago, whereas a second increase in oxygen levels to current atmospheric concentrations occurred 800 million years ago.
without a second jump in atmospheric oxygen concentration during the late Proterozoic, circa 800 million years ago (Figure 1), animals would never have evolved [14,15]. By showing the placement of cyanobacteria as a hub with connections between anaerobes and aerobes, network analyses provide further evidence for how the rise of oxygenic photosynthesis was the necessary catalyst to kick-start the aerobic revolution that progressed and continued to the present. Perhaps the most ambitious aspect of the study by Harel et al. [1] is their attempt to reconstruct the metabolic capabilities of the cyanobacterial progenitor. In order to grasp the difficulty of the question Harel et al. [1] have set out to answer, an analogy can be drawn from the more common example of birds and dinosaurs. It would be difficult to imagine what the ancient predecessors of birds, i.e. dinosaurs, would look like if we had no access to fossil data and had only ever seen modern crocodiles and birds. It would be a far stretch of the imagination to concoct the wide range of morphological differences that we know to have existed based on the dinosaur fossil record. Now, imagine doing this with an
ancient evolutionary relationship more than an order of magnitude older and microbial. Reconstructing the genomic and metabolic repertoire of ancestral cyanobacteria is no easy task. Impressively, the results extrapolated from the protein similarity networks provide evidence of various functions such as the biosynthesis of photosynthetic pigments, hydrogenase, DNA repair, and many other functions that make sense for a phototroph in the anoxic Archean world. It is important to keep in mind that it is impossible to definitively know the answer to the challenging questions that surround the origin of oxygenic photosynthesis and cyanobacteria. Without a time machine, we will never be able to perform genome sequencing of organisms that existed billions of years ago. In light of this humbling fact, novel studies such as Harel et al. provide keen insight that will continue to fuel the debate around this hotly contested field. Nonetheless, it is studies like this that will also help push the field forward and promote the discussion necessary to prompt scientists to come up with the next creative approach to addressing this incredibly difficult yet profoundly important question.
1. Harel, A., Karkar, S., Cheng, S., Falkowski, P.G., and Bhattacharya, D. (2015). Deciphering primordial cyanobacterial genome functions from protein network analysis. Curr. Biol. 25, 628–634. 2. Rye, R., and Holland, H.D. (1998). Paleosols and the evolution of atmospheric oxygen; a critical review. Am. J. Sci. 298, 621–672. 3. Shen, Y., Buick, R., and Canfield, D.E. (2001). Isotopic evidence for microbial sulphate reduction in the early Archaean era. Nature 410, 77–81. 4. Johnson, J.E., Webb, S.M., Thomas, K., Ono, S., Kirschvink, J.L., and Fischer, W.W. (2013). Manganese-oxidizing photosynthesis before the rise of cyanobacteria. Proc. Natl. Acad. Sci. USA 110, 11238–11243. 5. Schopf, J.W. (1993). Microfossils of the Early Archean Apex chert: new evidence of the antiquity of life. Science 260, 640–646. 6. Brasier, M.D., Green, O.R., Jephcoat, A.P., Kleppe, A.K., Van Kranendonk, M.J., Lindsay, J.F., Steele, A., and Grassineau, N.V. (2002). Questioning the evidence for Earth’s oldest fossils. Nature 416, 76–81. 7. Roger, A.J., and Hug, L.A. (2006). The origin and diversification of eukaryotes: problems with molecular phylogenetics and molecular clock estimation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 1039–1054. 8. Philippe, H., and Forterre, P. (1999). The rooting of the universal Tree of Life is not reliable. J. Mol. Evol. 49, 509–523. 9. Shih, P.M., Wu, D., Latifi, A., Axen, S.D., Fewer, D.P., Talla, E., Calteau, A., Cai, F., Tandeau de Marsac, N., Rippka, R., et al. (2013). Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc. Natl. Acad. Sci. USA 110, 1053–1058. 10. Abby, S.S., Tannier, E., Gouy, M., and Daubin, V. (2012). Lateral gene transfer as a support for the tree of life. Proc. Natl. Acad. Sci. USA 109, 4962–4967. 11. Iwabe, N., Kuma, K., Hasegawa, M., Osawa, S., and Miyata, T. (1989). Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc. Natl. Acad. Sci. USA 86, 9355–9359. 12. Gogarten, J.P., Kibak, H., Dittrich, P., Taiz, L., Bowman, E.J., Bowman, B.J., Manolson, M.F., Poole, R.J., Date, T., and Oshima, T. (1989). Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes. Proc. Natl. Acad. Sci. USA 86, 6661–6665. 13. Shih, P.M., and Matzke, N.J. (2013). Primary endosymbiosis events date to the later Proterozoic with cross-calibrated phylogenetic dating of duplicated ATPase proteins. Proc. Natl. Acad. Sci. USA 110, 12355–12360. 14. Planavsky, N.J., Reinhard, C.T., Wang, X., Thomson, D., McGoldrick, P., Rainbird, R.H., Johnson, T., Fischer, W.W., and Lyons, T.W. (2014). Low Mid-Proterozoic atmospheric oxygen levels and the delayed rise of animals. Science 346, 635–638. 15. Mills, D.B., Ward, L.M., Jones, C., Sweeten, B., Forth, M., Treusch, A.H., and Canfield, D.E. (2014). Oxygen requirements of the earliest animals. Proc. Natl. Acad. Sci. USA 111, 4168–4172.
Joint BioEnergy Institute, 5885 Hollis St, Emeryville, CA 94608, USA and Physical Biosciences Division, Lawrence Berkeley National Laboratory, One Cyclotron Rd, Berkeley, CA 94720, USA. E-mail: [email protected]
http://dx.doi.org/10.1016/j.cub.2014.12.046
