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Reactive Oxygen Species May Play an Essential Role in Driving Biological Evolution: the Cambrian Explosion As an Example, J JES-01206; No of Pages 9 JOURNAL OF ENVIRONMENTAL SCIENCES XX (2017) XXX– XXX Available online at www.sciencedirect.com ScienceDirect www.elsevier.com/locate/jes 1Q2 Opinion discussion 2Q1 Reactive oxygen species may play an essential role in driving 3 biological evolution: The Cambrian Explosion as an example 1 2,⁎ 2 2 Q44Q3 Dong Yang , Xuejun Guo , Tian Xie , Xiaoyan Luo 5 1. Gene Engineering and Biotechnology Beijing Key Laboratory College of Life Sciences, Beijing Normal University, Beijing 100875, China 6 2. State Key Laboratory of Environment Simulation, School of Environment, Beijing Normal University, Beijing 100875, China 7 910 ARTICLE INFO ABSTRACT 11 Article history: The Cambrian Explosion is one of the most significant events in the history of life; 15 12 Received 22 May 2017 essentially all easily fossilizable animal body plans first evolved during this event. Although 16 13 Accepted 26 May 2017 many theories have been proposed to explain this event, its cause remains unresolved. 17 14 Available online xxxx Here, we propose that the elevated level of oxygen, in combination with the increased 18 mobility and food intake of metazoans, led to increased cellular levels of reactive oxygen 19 27 Keywords: species (ROS), which drove evolution by enhancing mutation rates and providing new 20 28 Cambrian regulatory mechanisms. Our hypothesis may provide a unified explanation for the 21 29 Bilaterian Cambrian Explosion as it incorporates both environmental and developmental factors 22 30 Reactive oxygen species and is also consistent with ecological explanations for animal radiation. Future studies 23 31 Evolution should focus on testing this hypothesis, and may lead to important insights into evolution. 24 32 Metazoa © 2017 The Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences. 25 33 Published by Elsevier B.V. 26 3536 3734 3839 Contents 40 Introduction ............................................................. 0 41 1. Increased oxygen level before the Cambrian set the stage for animal evolution ..................... 0 42 2. Increased oxygen consumption generates more ROS and contributes to evolution .................... 0 43 3. Global environmental disturbances causing large-scale ecological oxidative stress .................... 0 44 4. ROS regulate key developmental genes and signaling pathways that affect cell renewal and differentiation ...... 0 45 5. The evolutionary lag between the digestive and excretory systems in early metazoans may also cause oxidative stress 0 46 6. An oxidative model for the evolution of early bilaterians .................................. 0 47 7. ROS may have broader implications in evolution ...................................... 0 48 8. Conclusions .......................................................... 0 49 Author disclosureUNCORRECTED statement .................................................... PROOF 0 50 Uncited reference .......................................................... 0 51 Acknowledgments ......................................................... 0 52 References .............................................................. 0 53 ⁎ Corresponding author. E-mail: [email protected] (Xuejun Guo). http://dx.doi.org/10.1016/j.jes.2017.05.035 1001-0742/© 2017 The Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences. Published by Elsevier B.V. Please cite this article as: Yang, D., et al., Reactive oxygen species may play an essential role in driving biological evolution: The Cambrian Explosion as an example, J. Environ. Sci. (2017), http://dx.doi.org/10.1016/j.jes.2017.05.035 2 JOURNAL OF ENVIRONMENTAL SCIENCES XX (2017) XXX– XXX 2013). Furthermore, because ROS are also important signaling 113 5455 Introduction molecules, their increased abundance could also provide new 114 regulatory mechanisms for development (Covarrubias et al., 115 56 Although the first animals may have evolved during the 2008). Therefore, we proposed that ROS may have been a 116 57Q5 Ediacaran Period (about 580 million years ago (mya)) or even central factor in the environmental, developmental and 117 58 earlier, essentially all easily fossilizable animal body plans ecological mechanisms that caused the radiation of early 118 59 emerged within about 35 mya in the early Cambrian (Marshall, bilaterians. In the following sections of this article, we will 119 60 2006; Briggs, 2015; Valentine, 2004; Butterfield, 2015). This discuss this model in greater detail. 120 61 phenomenon is called the Cambrian Explosion, and is one of 62 the most important evolutionary events in Earth history. 63 There have always been questions about the reliability of 1. Increased oxygen level before the Cambrian set 121122 64 fossil evidence, because of the incompleteness of the fossil the stage for animal evolution 123 65 record and conflicts with molecular clock estimates. However, 66 recent evidence strongly supports the conclusion that the Before the Great Oxygenation Event (GOE) at about 2.45 Ga, 124 67 Cambrian Explosion was a real evolutionary phenomenon as any oxygen molecules in the atmosphere were captured by 125 68 opposed to an artifact of taphonomy. The occurrence of trace oxygen sinks such as dissolved iron and organic matter 126 69 fossils is independent of the presence of hard parts, and can (Canfield, 2005, 1998; Holland, 2006). Between 1.8 and 127 70 provide information on soft-bodied animals that were rarely 0.85 Ga, the oxygen level in the atmosphere remained low, 128 71 preserved. Studies have shown that trace fossils became no more than 10% PAL (present atmospheric level) (Canfield, 129 72 larger and more complex throughout the Cambrian Period, 2005, 1998; Holland, 2006; Sperling et al., 2015; Mills and 130 73 which is consistent with the rapid radiation of animals Canfield, 2014). Some researchers have estimated that during 131 74 (Valentine, 2004). Although earlier molecular clock analyses much of the Proterozoic Eon, atmospheric oxygen could have 132 75 often conflicted with fossil data by suggesting many phyla been as low as 0.1% PAL (Sperling et al., 2015), in which case 133 76 evolved several hundred million years before the Cambrian, the oxygen content of seawater would have been exhausted 134 77 recent advances in molecular analyses have significantly as it passed from the sea surface downward to the seafloor, 135 78 reduced Precambrian divergence time estimates between and thus caused the deep-ocean anoxia (Canfield, 2005). 136 79 phyla (Lee et al., 2013; Erwin et al., 2011; Rota-Stabelli et al., Canfield and colleagues (Canfield, 2005, 1998; Holland, 2006) 137 80 2013), and current results from molecular analyses and are have shown that the oxygen content in the atmosphere and 138 81 more or less reconcilable with the fossil record. the anoxic conditions in the deep ocean could cause the 139 82 “ 140 One explanation for the Cambrian Explosion is that the rate buildup of H2S in the ocean, and form a so-called Canfield 83 of animal evolution may have been much higher during that Ocean”, which may explain why complex multicellular 141 84 period. One simulation study has indicated that rates of organisms did not evolve during this period of Earth's history 142 85 evolution would have to increase by a factor of five to recreate (termed the “Boring Billion”). 143 86 the observed divergences that were then compressed into Between 850 and 540 mya, there was a rapid increase in 144 87 35 million years (Levinton et al., 2004). Recent analyses of atmospheric oxygen content. The causes of this rise remain 145 88 molecular and morphological data of arthropods have suggested uncertain, although plausible explanations have been pro- 146 89 that their rates of evolution indeed increased by 4- to 5.5-fold in posed, such as increased burial of organic carbon associated 147 90 the early Cambrian (Lee et al., 2013). with continental breakup (Canfield, 2005, 1998; Holland, 2006). 148 91 Several possible mechanisms for the Cambrian explosion At the end of this period, the level of oxygen in the 149 92 have been proposed (Marshall, 2006; Valentine, 2004); some atmosphere was close to that of the present (Holland, 2006), 150 93 are based on environmental changes, such as increased which could lead to oxygenation of the deep ocean. A recent 151 94 atmospheric oxygen levels or Snowball Earth events. How- geochemical study on sedimentary rocks from the late 152 95 ever, it is difficult to directly correlate environmental change Ediacaran revealed that these rocks formed under a more 153 96 with new levels of developmental and morphological organi- oxygenated environment than the underlying Cryogenian 154 97 zation. Another theory is that the evolution of a new genetic deposits. This finding suggests that immediately before the 155 98 circuit was the primary cause. However, evidence suggests Cambrian Explosion, water of the deep ocean had already 156 99 that the genes governing bilaterian development evolved at transitioned from anoxic to fully oxygenated (Chen et al. 2015; 157 100 least tens of millions years before the Cambrian Explosion Johnston et al., 2012). 158 101 (Valentine, 2004). Finally,UNCORRECTED there are ecological explanations A high oxygen PROOF level is essential for metabolically active 159 102 whereby predation and grazing are suggested to have been animals. It is also necessary for synthesizing collagen. 160 103 the major causes of the rapid radiation of animals. Although Because collagen is essential for the formation of tissues, a 161 104 ecological factors
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