# The co-evolution of life and organics on earth:
Expansions of energy harnessing

Guo-Xin Sun, Song-Can Chen, Gang Li, Xiao-Ming Li, Long-Jun Ding, Brian

Reid, Philippe Ciais, Yong-Guan Zhu

► To cite this version:

Guo-Xin Sun, Song-Can Chen, Gang Li, Xiao-Ming Li, Long-Jun Ding, et al.. The co-evolution of life and organics on earth: Expansions of energy harnessing. Critical Reviews in Environmental Science and Technology, 2020, 51 (6), pp.603-625. 10.1080/10643389.2020.1734434. hal-04624420

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The co-evolution of life and organics on Earth: expansions of energy harnessing

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Guo-Xin Sunª, Song-Can Chenª, Gang Liᵇ, Xiao-Ming Liª, Long-Jun Dingª,

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Brian J. Reidᶜ, Philippe Ciaisᵈ, Yong-Guan Zhuª, ᵇ*

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ª State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China.

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ᵇ Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China.

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ᶜ School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, UK

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ᵈ Laboratoire des Sciences du Climat et de l'Environnement, CEA CNRS UVSQ, 91191 Gif-sur-Yvette, France.

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* Corresponding author. Phone: 86-10-62849328, E-mail: ygzhu@rcees.ac.cn.

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# The co-evolution of life and organics on Earth: expansions of energy harnessing

**Abstract:** The organic matter was absent prior to planetesimal formation (4.6 Gyr) but at present abundant in planetary environments. The aim of this study was to combine information about the organic inventory of the Earth, which is accompanied by the evolution of life. A variety of available free energy sources, including geochemical energy, sunlight, oxygen and fire have supported life evolution. In the meantime these energy sources have mediated the diversity and complexity of living organisms and resulted in a concomitant increase in the diversity and complexity of organic matter, including microbial-, plant-, fire-, and human derived organics. The change of the diversity and complexity of organic matter (microbial-, plant-, fire- and human-derived organics) have in-return significantly influenced Earth's carbon cycle, planetary climate and ecosystems. Overall, energy harnessing and conservation of life entwined and expanded the evolutional histories of life and organic molecules on the planet. Considering the key role of organics on the stability of the oxygen level of the atmosphere, temperature, the tectonic rise of continents, and global habitability, the changing characters of organics over geologic time had an important shaping influence on Earth's geochemical cycles.

**Keywords:** organic matter; life; energy harnessing

## 1. Introduction

Life is processes of generating reduced organic compounds from carbon dioxide as well as the harnessing of environmental energy. Over the course of Earth history, the harnessing of free energy by organisms has had a dramatic impact on the geosphere, including minerals and
organics (Dietrich et al., 2006; Grosch & Hazen, 2015; Judson, 2017), shaped the whole
trajectory of life evolution. As a direct consequence of a coevolving geosphere and biosphere,
the Earth's crust has changed greatly over billions of years. The origin and evolution of
organic compounds on the planetary environment are compelling because of their potential
role in the origin of life and sustaining microbial communities (Lazcano & Miller, 1996;
McDermott et al., 2015; Schönheit et al., 2016). Carbon lies at the heart of carbon-based life
forms and provides unparelleled potential for earth evolution. The origin of life is
inextricably linked to the behavior of carbon (Hazen, 2019). The evolution of organics is
coupled with the evolution of life, which is expanded with a variety of available free energy
sources (Judson, 2017). Collectively, these linkages have mediated the generation and
transformation of soils and sediments. Here we review the origin and evolution of organics
on Earth, and their relationship with diversification and expansion of energy utilization and
with biological and geological development.

## 2. The prebiotic organics

Earth accreted 4.56 billion years (Gyr) ago from largely homogeneous material (Judson, 2017; Hazen et al., 2013). With the dissipation of thermal energy produced by compaction, radiation, and impacting meteorites, the Earth cooled. About 4.4 Gyr ago patches of a rocky scum had solidified and eventually separated into core, mantle, and crust (Mojzsis, 2010).

Water vapor condensed as rain and formed early oceans and seas (Wilde et al., 2001; Rosing et al., 2006; Hazen et al., 2013). The early ocean was a reservoir of inorganic elements, and also a reservoir of potential free energy in the form of protons. Before the emergence of life
on early Earth at ~3.8 Gyr (Dodd et al., 2017), these prebiotic organics were either
synthesized abiotically on the Earth itself or synthesized extraterrestrially and then delivered
to the Earth (Hayes et al., 1967; Dalai et al., 2016). A wide range of organic compounds
including amino acids, monocarboxylic acids, sugars, nucleobases, and membrane-forming
lipids have been synthesized in prebiotic conditions simulation experiments (McCollom,
2013). Questions remain, however, concerning whether the conditions that allow synthesis of
these compounds in the laboratory accurately simulate those that might have been present on
the early Earth (McCollom, 2013; Dalai et al., 2016). High concentrations of the reactants,
water pH and ambient temperature are of central importance in experimental abiotic synthesis
of organics. The extreme environments (highly acidic condition) of early Earth presented
severe limitations with respect to their potential for prebiotic chemistry because of stability
and synthetic pathway issues associated with temperatures and pH (Bada, 2013). It has been
claimed that autocatalytic metabolic-like reactions can overcome these limitations (Huber &
Wächtershäuser, 1998). The micro-conditions in the hydrothermal systems supposedly could
drive abiotic syntheses of organics (McCollom & Seewald, 2007; McDermott et al., 2015).
Prebiotic syntheses could have taken place in a variety of geochemical environments that
may have existed on the primitive Earth, although this has never been demonstrated using
plausible geochemical conditions (Box 1). Highly reducing fluids such as deep-sea
hydrothermal fluids have the potential for abiotic reduction of dissolved inorganic carbon to
produce organic compounds (Shock, 1990; Shock & Schulte, 1998; Seewald et al., 2006;
McDermott et al., 2015). There is also increasing evidence that supports an abiotic origin for
CH₄ and other low-molecular weight reduced organic compounds in ultramafic-hosted
hydrothermal systems (Charlou et al., 2002; McCollom & Seewald, 2007; Proskurowski et al., 2008). Given the scarcity of suitable abiotic regime the yield prebiotic organics on the early Earth would have been very small (Lollar et al., 2002).

Besides the abiotic synthesis of organic molecules on the young Earth driven by various energy sources such as UV radiation in sunlight, cosmic rays, X-rays, hypervelocity impacts, volcanic eruptions with lightning, geothermal heat, and redox gradients, the total inventory of organics would have included exogenous sources (the interstellar medium, interplanetary dust, asteroids, comets, meteorites) (Dalai et al., 2016; Kwok, 2016; Sahai et al., 2016; Sandford et al., 2016). It has long been speculated that Earth accreted prebiotic organic molecules from impacts of carbonaceous asteroids and comets during the period of 4.5 Gyr to 3.8 Gyr ago (Chyba et al., 1990; Chyba & Sagan, 1992; Botta & Bada, 2002) because the exogenous delivery has showered the Earth (Pizzarello & Weber, 2004). Polyhydroxylated compounds (such as sugars, sugar alcohols and sugar acids) are formed under interstellar conditions via photolysis of small molecules (e.g. CO, NH₃ and H₂O) and are therefore present in meteorites (Agarwal et al., 1986; McDonald et al., 1996; Cooper et al., 2001). The carbonaceous component of interplanetary dust could be up to 50 wt% (Ehrenfreund & Charnley, 2000; Dalai et al., 2016). This dust material has been reported to contain simple aliphatic, aromatic compounds, macromolecular polyaromatic hydrocarbons (Ehrenfreund & Charnley, 2000; Dalai et al., 2016), amino acids and other organic compounds (Cooper et al., 2001) that are vital to the origin of life. Tens of thousands of tons of interplanetary dust particles enter the Earth's atmosphere annually, and the rate may have been much greater on early Earth (Kwok, 2016). It was estimated that Earth was also accreting intact cometary organics at a rate of at
least $10^9$ to $10^{10}$ g per year at 4.5 Gyr (Chyba et al., 1990). Organics delivered from space
comprising as much as perhaps 10% of the Earth's modern biomass by weight (Sephton, 2002;
Schönheit et al., 2016) estimated that about $1.0×10^{21}$ mol of reduced carbon were probably
delivered to the surface of Earth by asteroids (4.4 - 3.8 Gyr) (Catling et al., 2001; Hayes &
Waldbauer, 2006).

### 3. Geochemical energy

Organics underpin the co-evolution of Earth's geosphere and biosphere. Organics likely
played critical roles in the origin of life, and, in return, life has played a symbiotic role in the
production and cycling of organics. The emergence of life on Earth gave rise to a source of
organics in both abundance and diversity. Life began very early, before 3.8 Gyr (Des Marais,
2000; Nisbet & Sleep, 2001). Two main theories, based on heterotrophic versus
chemoautotrophic metabolisms, have emerged to account the origin and early evolution of
life (Ferry & House, 2006; Herd et al., 2011; Schönheit et al., 2016). Theories for autotrophic
origins posit that the first cells satisfied their carbon needs from CO (Say & Fuchs, 2010;
Fuchs, 2011; McDermott et al., 2015). While the heterotrophic theory proposes that life arose
from an "organic soup" of diverse preexisting molecules which were delivered from space or
abiotically formed (Lazcano & Miller, 1999; Bada & Lazcano, 2002). Regardless of the
chemoautotrophic or heterotrophic origins, organisms had evolved to take advantage of the
available energy to fuel their proliferation and to produce new organic matter.

At this time in Earth history, oxygen was at trace levels (Canfield et al., 2006), so the
first ecosystems must have existed in an anoxic world and their activities were driven by
anaerobic metabolisms (Canfield et al., 2006; Judson, 2017). The proposed emergency of life under anoxic geothermal environments implies that life started not as a planetary but as a local phenomenon. It was reported that metabolisms of early anaerobic ecosystems were probably 2–3 orders of magnitude less active than the present biosphere (Des Marais, 2000). Given these factors and the probable limits on accessing the most limiting chemical compounds, various ecosystems most likely existed in relative isolation (Canfield et al., 2006).

Noting that the energy budget of Earth places strict constraints on fluxes of basic components required for chemoautotrophic life, life was unable to influence the Earth's carbon cycle in any significant way in the absence of photosynthesis (Rosing et al, 2006). Geochemical models (Bergman et al., 2004; Berner, 2009) suggest that the productivity of the biosphere before it was powered by sunlight harvested through photosynthesis, would have been at least a thousand times less than it is today (and maybe one million times less). Combined continental reservoirs of organic carbon probably grew very slowly through the Earth history and were still negligible before 3.5 Gyr ago (Godderis & Veizer, 2000; Canfield et al., 2006). Owing to the low productivity of the non-photosynthetic early biosphere, its initial influence upon the life-energy-organic dynamic would have been small (Canfield et al., 2006; Sleep & Bird, 2007; Judson, 2017).

## 4. Sunlight

The greatest energy source in the surface environment of the Earth is sunlight. Today the average solar energy flux to Earth surface is 340 W/m² (Rosing et al., 2006). The early Sun
was fainter and solar luminosity was probably a quarter to a third less than the present day (ca 151 152 250 W/m² at 4.0 Gyr; Sagan & Chyba, 1997; Nisbet & Sleep, 2001).

It is reported that by ca. 3.7 Gyr (Fig. 1) (Rosing, 1999; Pecoits et al., 2015; Nutman et al., 2016), photosynthetic organisms emerged to harness the energy in sunlight to drive chemical reactions. When the biosphere developed photosynthesis, living organisms acquired the ability to absorb solar energy and convert a fraction of it into chemical free energy (Rosing et al., 2006). Photoautotrophs acquired the ability to build up gradients in chemical potential, rather than just exploiting existing gradients, as was the fate of their chemoautotrophic predecessors. With evolution of photosynthesis, energy resources available for lives became several orders of magnitude larger than that available from oxidation-reduction reactions (chemoautotrophic primary production) associated with hydrothermal activities (Des Marais, 2000; Rosing, 2005; Rosing et al., 2006). The development of photosynthesis allowed life to escape the hydrothermal setting (Nisbet & Sleep, 2001). Energy harvested from sunlight, therefore, enhanced the rates of autotrophic carbon fixation, and carbon burial in anoxic environments. The primary productivity of the photosynthetic world was estimated to be 10,000 times higher than those of non-photosynthetic ecosystems (Sleep & Bird, 2008; Summons & Hallman, 2014), although the rates would have been significantly lower than the present (Summons & Hallman, 2014). The earliest photosynthetic organisms performed anoxygenic photosynthesis, and were dependent on mineral sources as electron donors, but relieved the energy constraints to perform reduction of organic compounds (Olson & Blankenship, 2004; Rosing et al., 2006). The genesis of photosynthesis had irreversible consequences for Earth surface environments
173 whether it was oxygenic or anoxygenic.

174 Estimates suggest that anoxygenic phototrophs increased the flux of carbon through the
175 biosphere and the most active ecosystems were probably driven by the cycling of Fe²⁺, with
176 the oxidation of Fe²⁺ yielding potentially the highest rates of primary production (Canfield et
177 al., 2006). The importance of hydrogen as an early fuel for anoxygenic photosynthesis has
178 also been emphasized by Olson, (2006), and may have been sufficiently abundant in the early
179 Earth to drive CO₂ reduction. Other dynamic ecosystems would have also been driven by the
180 microbial cycling of sulfur and nitrogen species, but these would have been considerably less
181 active in comparison with those based on iron and hydrogen as electron donors to reduce CO₂
182 (Canfield et al., 2006). For all the ecosystems mentioned above, the production rates of
183 organics were considerably less than those of today. The primary production rates of total
184 carbon at 3.8 Gyr ago were estimated as 2.8×10¹⁴ mol yr⁻¹. Organic carbon accounted for
185 14% of the total carbon. This primary production estimate is 14 times lower than present rates
186 (4.0×10¹⁵ mol yr⁻¹) (Canfield et al., 2006). Considering that prokaryotic life was flourishing
187 and presumably widespread in the biosphere, organics must have been completely
188 microbially derived, which produces more labile organic matter with high H/C (the degree of
189 aliphatic character) and low O/C or (O + N)/C (the degree of polar character) ratios (Qiu et al.,
190 2014) such as lipid-, protein-, and amion sugar-like products (Fig. 2) (Brocks et al., 1999;
191 Grannas et al., 2006; D'Andrilli et al., 2015).

192 **5. Oxygen**

193 As the third most energetic oxidant, oxygen reduction provides the largest potential
source of energy per electron transfer, except for the reduction of chlorine and fluorine (Catling & Claire, 2005). Given the much less abundance of both chlorine and fluorine (several orders of magnitude less than oxygen) and their high reactivity with organics, their energy cannot be harnessed for life. On account of chemical sinks (such as reduced geothermal outflows and rock weathering) greatly exceeded the abiotic sources of oxygen (UV photolysis of water) ambient oxygen levels were insignificantly low (approximately $10^{-14}$ of present atmospheric $O_2$ levels) before oxygenic photosynthesis arose (Rosing et al., 2006; Buick, 2008). With the evolution of more advanced oxygen producing photosynthetic pathways, life became independent of both energy and reducing power derived from mineral substrates (Rosing et al., 2006). Geologic evidence suggests that oxygenic photosynthesis originated before 2.8 Gyr (Fig. 1) (Des Marais, 2000). At present cyanobacteria are the most numerous (~$10^{27}$) among all organisms performing oxygenic photosynthesis (among green plants, phytoplankton and cyanobacteria) (Catling & Claire, 2005). Cyanobacteria raised oxygen levels in the atmosphere (> $10^{-3}$ present atmospheric $O_2$ level) by around 2.32 Gyr. This planetary change to atmospheric $O_2$ levels is referred to as the Great Oxidation Event (GOE) (Kopp et al., 2005; Buick, 2008). Oxygenic photosynthesis was clearly well established by this time (Schirrmeister et al., 2013).

The stratospheric ozone layer seems to have been created at 2.3 Gyr (Goldblatt et al., 2006). The formation of the ozone layer was facilitated by $O_2$ levels rising to 1-3% of present levels; at these levels, photolysis of oxygen (yielding reactive oxygen radicals) was sufficiently frequent for an ozone layer to be produced, which shielding life from short-wave UV-radiation (200-300 nm) and was suitable for life to expand on the continents (Goldblatt et
al., 2006). Beyond the energetic limitations, defined by the availability of oxygen, the only limiting factors for life from the environment became the availability of bio-essential elements (Rosing et al., 2006). The increase in the oxygen content of the atmosphere and ocean driven by photosynthesis increased chemical weathering rates (Shields, 2007), which in turn increased nutrient (e.g. phosphorus, partly nitrogen, and iron) availability (Shields, 2007; Kump, 2010). The far-reaching impact of the GOE cannot be emphasized enough: it changed Earth's history by enabling the evolution of aerobic life, an explosion in the biosynthesis of organics and this underpinned the opportunity for organics to be generated and to proliferate in large quantities on a planetary scale.

Oxygenic photosynthesis is by far the most efficient mechanism for harvesting solar energy (Rosing et al., 2006). The GOE changed Earth's history by enabling the evolution of aerobic life (eukaryotes) and the emergence of the lineage that would eventually produce land plants. On Earth, aerobic metabolism provides about an order of magnitude more energy for a given intake of food than anaerobic metabolism (Judson, 2017). As a consequence of energetic limitations, life without O₂ as a strong electron acceptor, well mixed in the atmosphere and the surface ocean, could not grow large and complex (Lane & Martin, 2010). On account of prohibitively low growth efficiencies and energetic limitations anaerobes do not grow beyond the complexity of uniseriate filaments of cells (Schulz & Jørgensen, 2001; Catling & Claire, 2005). The oxygenated atmosphere and ocean enabled the evolution of more complex life (Payne et al., 2009; Dahl et al., 2010; Kump, 2010). The maximum body size of organism has increased by 16 orders of magnitude since emergence of life; this transition occurred via two discrete steps (Payne et al., 2009). The first was the emergence of
238 eukaryotic cell (~1.9 Gyr) and the second was eukaryotic multi-cellularity (0.6-0.45 Gyr).

239 These two steps coincide or slightly postdate with increases in atmospheric oxygen levels

240 (Payne et al., 2009). The evolution of Earth's biota is intimately linked to the oxygenation of

241 the atmosphere and the oceans (Dahl et al., 2010). This atmospheric oxygenation correlates

242 with the diversification and radiation of vascular plants on the continents (Gensel, 2008) and

243 the oxygenation of the oceans correlates with the expansion of large predatory fish (Bambach,

244 2002). This evolution significantly enhanced the burial of reduced carbon and was accompanied

245 by the accumulation of organic matter (Fig. 1).

246 There exists a striking temporal overlap between the atmospheric oxidation and the rise

247 of the continents (Dietrich et al., 2006; Rosing et al., 2006). Continent shaping was probably

248 associated with burial of organic matter fixed by oxygenic photosynthetic organisms under

249 sediment eroded from the new blocks of crust (Des Marais et al., 1992; Dietrich et al., 2006).

250 The rifting of large continental plates on the global scale probably promoted the development

251 of extensive anoxic basins favorable for organic preservation (Des Marais et al., 1992),

252 promoted the burial of refractory plant material (e.g., lignin, cellulose, and of other refractory

253 organic compounds) (Berner, 2009).

254 The emergence of larger, and less easily degradable organic molecules related to

255 eukaryotic diversification thus enhanced the burial of organic matter and its diversity. One of

256 the most unique and pervasive biological characteristics of organic matter in terrestrial

257 environments is the predominance of sources from vascular plants (Oades, 1993). For

258 example, during the Carboniferous period (360-300 Ma), oxygen in atmosphere rose to
between 30 and 35% (Berner et al., 2003; Hsia et al., 2013), coinciding with the appearance

giant vascular plants, fern-dominated forests (Shear, 1991). Fern are lignin rich plants that

contain > 40% of lignin than modern plants (~20%) (Robinson, 1990), and this lignin was
difficult to decompose until organisms like fungi evolved and effective degradation occurred

until 200 million years after fern plant emergence (Robinson, 1990). The rise of ligniferous

plants and low lignin breakdown (due to the rare or absence of lignolytic organisms)

contributed to increased terrestrially derived organic matter burial through inhibited
decomposition (Robinson, 1990; Berner et al., 2003). The spread of vascular plants in the

terrestrial environment increased the diversity of organic matter, including plant-derived

polysaccharides such as cellulose and phenolic compounds such as lignin (Benner et al., 1984;

McLatchey & Reddy, 1998). These organic compounds are characterized by less labile, more

recalcitrant chemical nature with H/C <1.5 (Fig. 2) (D'Andrilli et al., 2015).

271 6. Fire

272 To trigger wildfire, all of three conditions must be met (Scott & Glasspool, 2006). Firstly,
273 a source of ignition—such as lightning strikes, meteor strikes and volcanic activity.
274 Throughout the Earth history, these have been abundant. Lightning is the pre-eminent source
275 of heat for the ignition of fossil wildfires. Lightning strikes occurred more than 1.4 billion
276 lightning strikes per year owing to its global frequency (44 ± 5 strikes/s) (Christian et al.,
277 2003), of which an appreciable number ignite wildfires. Secondly, sufficient amount of
278 oxygen became present in the atmosphere. Assuming current atmospheric pressure, at least
279 16% oxygen is the minimum concentration in order for plants to ignite and for fire to be
self-sustaining (Belcher & McElwain, 2008; Belcher et al., 2010). For most of Earth's history, oxygen levels have been lower than this threshold until 0.35 Gyr (Scott, 2000; Scott et al., 2013). Thirdly, fire requires fuel. The earliest land plants (embryophytes) evolved from charophycean green algal ancestors (Steemans et al., 2009) at approximately 0.47 Gyr (Berner, 2009). The appearance of vascular plants on land occurred around 0.42 Gyr ago, although they were tiny and leafless (Lenton, 2001; Banks et al., 2011). All three conditions were met and fire activity has begun to influence the Earth system and the cycling of organic matter.

The evolution of plants increased the atmospheric oxygen concentration, contributing to increase the amount of oxygen for fire formation. In the meantime, plants provide the fuel for fire. Fire activity would be globally distributed, even in wetter climatic areas as when oxygen reaches levels >30%, fire can be sustained (Scott & Glasspool, 2006). The Carboniferous period was characterized as a 'high-fire' world due to elevated levels (35%) of oxygen (Berner, 2006; Glasspool & Scott, 2010). A diverse vegetation provided a major and extensive fuel resource although vast swamps were present on the continents (Berner, 1999). Significantly enhanced fire activity continued during the Cretaceous (145-65 Ma) (Belcher et al., 2010), and is hypothesized to be associated with the rise of angiosperms during this period (Bond & Scott, 2010; Bond & Midgley, 2012).

Fire has had both geological and biological impacts on ecosystems. Fire regimes drive the evolution of plant traits, such as thick bark (Bond et al., 2005; Pausas & Keeley, 2009; Keeley et al., 2011); the initial spread of flowering plants (Bond & Scott, 2010); faunal
abundance and diversity such as ants (Moreau et al., 2006); shape biomes (Crisp et al., 2010, 2011; Scheiter et al., 2012); affect soils quality and nutrient cycling such as the carbon, oxygen and phosphorous cycles; promote biodiversity (Bond & Keeley, 2005). Due to the fire integration to ecosystem function and maintenance (Keeley & Rundel, 2005; Edwards et al., 2010), pyrophilic grasslands and savannas such as C₄ grasslands expanded and replaced woodlands (Keeley & Rundel, 2005; Hoetzel et al., 2013).

The emergence of fire in terrestrial environment likely had a profound effect upon the compositions and dynamics of organic carbon. Furthermore, fire contributes new material to the Earth—pyrogenic carbon or fire-derived organic matter (partly charred organic matter including black carbon, charcoal and soot) (Lenton, 2013; Judson, 2017). Glinka, (1914) described that “there was almost no soil profile in which charcoal particles did not occur in the upper horizon” (Bird et al., 2015). In modern peats, charcoal may constitute 4% of the total volume. In the Carboniferous, charcoal represented more than 20% of dead organic matter (Scott et al., 2013). It was recently estimated that 3-5 million km² of the Earth surface are burned by wildfires annually (Jones et al., 2019) and approximately 116-385 Tg/yr of pyrogenic carbon are now produced globally by fires (Santin et al., 2016). Pyrogenic carbon can represent a significant proportion of total organic carbon in the environment: ranging from 2% to 60% of the total soil organic carbon in terrestrial systems (Singh et al., 2012; Reisser et al., 2016). Santin et al. (2016) provided a global assessment of pyrogenic carbon fluxes. Accounted for 8 to 27% of the annual production of pyrogenic carbon were inputted to oceans from rivers and most of pyrogenic carbon was deposited on the continental shelf (Santin et al., 2016). These reports indicate that pyrogenic carbon is a significant component
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in both terrestrial and oceanic carbon storage (Preston & Schmidt, 2006). Moreover,
pyrogenic carbon has a condensed aromatic structure with low H/C and O/C ratios; it is
therefore recalcitrant (D'Andrilli et al., 2015). It has been established that pyrogenic carbon
can persist in soils and sediments for millions of years and thus it plays an important role in
the global carbon inventory of the Earth and fluxes between reservoirs over long time scales
(Schmidt & Noack, 2000; Forbes et al., 2006; Scott, 2010). Human activities that suppress
the production of pyrogenic carbon have significantly disturbed the pyrogenic carbon cycle
(Bowman et al., 2011; Andela et al., 2017).

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The advent of anthropogenic fire was a revolutionary event in Earth history because fire
technology has significantly influenced the biosphere over the last 10,000 years (Box 2)
(Raupach & Canadell, 2010). Fire gave protection, extended the range of food, and expanded
adaptation to different environments on Earth (Froestad & Shearing, 2017). Fire plays a
pivotal role in the clearing of forests to create permanent fields with the development of
sedentary agriculture-based societies during the Holocene (Bowman et al., 2013). During the
late Quaternary humans have dramatically altered fire regimes around the globe, which is
largely dependent on fossil fuels, both directly and indirectly. The production and existence
of pyrogenic carbon underpin the significant perturbations of the carbon cycles both, on long
(million year) (Berner, 1999; 2003) and on short (thousand year) timescales. The application
of fire by humans, especially the fossil fuel burning, has accelerated both long- and
short-term carbon cycles through anthropogenical alternation of carbon fluxes, the increase of
CO₂ in the atmosphere, and global warming (Berner, 1999). Organic aerosols such as soot
from fire smoke in Earth's atomsphere is an important contributor to global climate change

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345 by absorbing heat and warming the air (Bond et al., 2013; Berner, 2003; Johansson et al., 346 2018).

347 Life is a process of harnessing energy to maintain states far from thermodynamic 348 equilibrium, leading to an energy flow through the biosphere (Raupach & Canadell, 2010). 349 Any reduction of an energy source could cause a corresponding contraction in the biosphere 350 and drop in the rate of global organic matter burial. In the traditional “big five” mass 351 extinctions oceanic anoxic events (due to the worldwide reduction of oxygen) have coincided 352 with four of these mass extinctions, especially, the end-Ordovician (Zhang et al., 2009), the 353 Late Devonian (Goddéris & Joachimski, 2004), the end-Permian (Wignall & Twitchett, 1996; 354 Grice et al., 2005), and the end-Triassic (Isozaki, 1997). Thus, rapid declines in atmospheric 355 O₂ have been proposed to have a major influence upon mass extinction events. For example, 356 in the most severe extinction (loss of as much as 95% of all species on Earth) that occurred in 357 the Late Permian (~251 Mya) (Benton & Twitchett, 2003; Grice et al., 2005; Chen & Benton, 358 2012), the oxygen level (at 30% or more in the Carboniferous period) fell dramatically to 359 13% in the late Permian and the early part of the subsequent Triassic (Lane, 2007). One 360 factor in the last mass extinction (end-Cretaceous) may be the prevention of sunlight from 361 reaching the surface of the Earth due to the dust, soot or aerosols in the atmosphere ejected by 362 the Chicxulub asteroid impact (Kring, 2007).

363 The sudden mass mortality of the terrestrial and marine organisms irreversibly 364 reorganized the global carbon cycle (Caplan & Bustin, 1999; Berner, 2002). A drop in burial 365 fluxes for global organic carbon is coincident with the abrupt biota change at the time of late
366 Permian (Berner, 2005) and the end-Cretaceous mass extinctions (D'hondt et al., 1998). Such
367 a reduction in the organic flux could have been a natural consequence of the ecosystem
368 reorganization that resulted from the mass extinctions.

369 **7. Conclusions**

370 The amount and proportion of pyrogenic carbon in total organic carbon on Earth are
371 expected to increase, which changed the diversity and complexity of organic matter on Earth.
372 The change of the diversity and complexity of organic matter (microbial-, plant-, fire- and
373 human-derived organics) have in-return significantly influenced Earth's carbon cycle,
374 planetary climate and ecosystems. The long-term organic carbon cycle has dominant
375 influenced the levels of atmospheric oxygen and carbon dioxide over a multimillion-year
376 time scale. The levels of atmospheric carbon dioxide and oxygen were mainly mediated via
377 weathering of organic matter on the continents, the burial of organic matter in sediments, and
378 the thermal breakdown of organic matter at depth. The increased oxidation of organic carbon
379 to carbon dioxide by weathering and thermal breakdown results in the O₂ consumption and
380 CO₂ production. The burial of organic matter in sediments leads to an increase in atmospheric
381 O₂ and a decrease of atmospheric CO₂ due to a net excess of photosynthesis over respiration
382 (Berner & Caldeira, 1997; Berner, 1999). Current burning of fossil carbon results in a
383 decrease of atmospheric O₂ by about 2 ppm per year (Keeling and Manning, 2014). The
384 fluctuation of atmospheric levels of O₂ and CO₂ would change the planetary climate,
385 temperature, precipitation (enhanced atmospheric CO₂ leads to a warmer and wetter climate
386 via the greenhouse effect), resulting in the evolution of biology. An integrated view of
387 assessing the role of the change of diversity and complexity of organic matter is required. A
388 full understanding of the role of pyrogenic carbon on planetary climate and ecosystems can
389 provide us with new opportunities for mitigating climate change.

390 If the development of life-energy-organic dynamics on other life-planet systems have
391 paralleled those on Earth (i.e. microbial-, plant-, fire-derived and anthropogenic organics),
392 then it follows that by analyzing the type of organics in their soils or rocks the evolution of
393 life-energy-organic histories/dynamics can be speculated upon (Hazen, 2019). For example, if
394 the soils or meteorites from another planet have only simple organic molecules it might be
395 inferred that the planet is in a prebiotic (or early life) stage. In contrast, where the soils or
396 meteorites from a planet have plant-derived or pyrogenic carbon, like Mars (Lin et al., 2014),
397 there exist implications for a possibly complex biosphere being present. Given, the entwined
398 evolution of life, energy utilization and organics there exist the possibility to evidence the
399 development of life elsewhere in the universe though assessment of organic matter profile
400 and the fingerprint they provide of biotic diversification.

401

402 Acknowledgements

403 This project was financially supported by the Natural Science Foundation of China (No.
404 41571130062), National Key Research and Development Program of China
405 (2017YFD0800303).

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830

831

832
833 Box 1 Abiotic Synthesis of Organic Compounds in Hydrothermal

834 Environments

835 Since the discovery of deep-sea hydrothermal systems in the late 1970s**Error! Reference source not found.** (Corliss et al., 1979), there has been keen interest in the origin of life in

836 these environments. The concept that deep-sea hydrothermal systems as sites of abiotic

837 organic synthesis is based largely on their strongly reducing chemical environments. Based

838 on geological observations as well as theoretical and experimental constraints, the theory

839 received support as having the potential for abiotic synthesis of organic compounds within

840 hydrothermal environments (Charlou et al., 2002; Martin et al., 2008; McDermott et al.,

841 2017). The abiotic formation of organic compounds in geologic systems involves the abiotic

842 reduction of dissolved inorganic carbon (ΣCO₂ = CO₂ + HCO₃⁻ + CO₃²⁻) to organic

843 compounds by dissolved H₂ produced by serpentinization, which can be expressed by the

844 following reaction (McCollom & Seewald, 2007):

845 CO₂ + H₂ → CH₄ + C₂H₆ + C₃H₈ + C₆H₉ + ... + H₂O

846 The synthesis of CH₄ and organics from H₂ and CO₂ releases energy. Geothermal energy is

847 transferred into chemical energy in the form of organic compounds. These reactions take

848 place readily on the Earth. Geochemistry thus offered fresh chemical, energetic, and

849 thermodynamic perspectives on biochemical origins (Martin, 2012).

850
852

Box 2 Fire and Hominins

853

854

855

856

857

858

859

The use of fire is a defining feature of humans with reliable records of fire use by hominins dated at 1 million years (Myr) ago (Berna et al., 2012; Bowman et al., 2013). The habitual use of fire for preparing food about 0.400 Myr (Roebroeks & Villa, 2011; Sandgathe et al., 2011) supported the larger human brains (Carmody & Wrangham, 2009) and relatively small gut given body size (Milton, 1999). Fire was a central evolutionary force and cooked diets tend to provide more energy for growing energy-expensive brains (Roebroeks & Villa, 2011).

860

861

862

863

864

865

866

867

868

With the harnessing of fire and the technological explosion, fire was replaced by the internal combustion engine. Considering that most of the energy used by human beings comes from the combustion of fossilized organic matter it might be asserted that humans have become the most important evolutionary force on the planet (Palumbi, 2001) considering most of the energy used by human beings comes from the combustion of fossilized organic matter. Industrial-scale use of energy flows from fossil carbon have significant effects on the climate, atmosphere, hydrosphere, and on global biogeochemistry (Gillings et al., 2015). These changes have altered the carbon and energy cycle in the Earth system, leading to the new epoch: the “Anthropocene”.

869

870

871

Many kinds of man-made organics such as synthetic polymers were produced and delivered into the environment. One of the most ubiquitous polymer is debris of plastics, which was produced in large quantities after World War II (Carpenter & Smith, 1972). Jambeck et al. (2015) reported that 275 million metric tons of plastic waste was generated in 2010 and 5 ~ 13 million tonnes of plastic have been transported to the ocean. Plastic

872

873
874

fragments are stable and highly durable, potentially lasting hundreds to thousands of years

875

(Barnes et al., 2009; Cózar et al., 2014). Thus, like the emergence of lignin with the

876

appearance of vascular plants on land (~420 Mya; Lenton, 2001; Banks et al., 2011) or

877

pyrogenic carbon (420 Mya; Cressler, 2001; Bird et al., 2015) the emergence of plastics

878

marks the beginning of a new era in the evolution of organics on Earth (Wu et al., 2017,

879

2019a, b).

880

881
882 Figure legends

883

884 Fig. 1 Quantity of organic carbon in the crust against age according to references (Des Marais et al., 1992; Hayes & Waldbauer, 2006). PAL: present atmospheric level. The variety of energy sources, e.g. geochemical energy, sunlight, oxygen and fire, to support the evolution of life.

887
888 Fig. 2 The derivation and characteristics of organic matter from asteriods, microbes, plants, fires and humans.

890

891
<figure><img src="image_2.png" /><figcaption>Figure 1</figcaption></figure>

893

894

895
<figure><img src="image_3.png" /><figcaption>Figure 2</figcaption></figure>

896

897

898