Evolving paradigms in biological carbon cycling in the ocean

44 45 Carbon is a keystone element in global biogeochemical cycles. It plays a fundamental role in 46 biotic and abiotic processes in the ocean, which intertwine to mediate the chemistry and redox 47 status of carbon in the ocean and the atmosphere. The interactions between abiotic and 48 biogenic carbon (e.g., CO 2 , CaCO 3 , organic matter) in the ocean are complex, and there is a 49 half-century-old enigma about the existence of a huge reservoir of recalcitrant dissolved 50 organic carbon (RDOC) that equates to the magnitude of the pool of atmospheric CO 2 . The 51 concepts of the biological carbon pump (BCP) and the microbial loop (ML) shaped our 52 understanding of the marine carbon cycle. The more recent concept of the microbial carbon 53 pump (MCP), which is closely connected to those of the BCP and the ML, explicitly considers 54 the significance of the ocean's RDOC reservoir and provides a mechanistic framework for the 55 exploration of its formation and persistence. Understanding of the MCP has benefited from 56 advanced “omics”, and novel research in biological oceanography and microbial 57 biogeochemistry. The need to predict the ocean’s response to climate change makes an 58 integrative understanding of the BCP, ML and MCP a high priority. In this review, we 59 summarize and discuss progress since the proposal of the MCP in 2010 and formulate research 60 questions for the future. 61 62


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Understanding of the ocean's carbon cycle in the late 20 th century was largely promoted by the 129 biological carbon pump (called "soft tissue pump" in Volk and Hoffert, 1985) and the 130 microbial loop (Azam et al., 1983). The term "pump" was initially used to refer to the 131 movement of carbon against a concentration gradient between the surface ocean and the deep 132 ocean (Volk and Hoffert, 1985). Both concepts find their roots in Dugdale and Goering (1967), 133 who recognized new (BCP) and regenerated (ML) production in the ocean.  also change the BCP leading to the next question: (4) How will the biological pump respond to 154 the consequences of increased carbon input combined with warming?" (Passow and Carlson,155 2012). One scenario suggests that in the coming decades decreasing phytoplankton cell size 156 will decrease the downward POC flux from the surface ocean, while changes in zooplankton 157 community structure will decrease the downward POC flux in subsurface waters (Boyd, 2015). 158 However, other predictions suggest alternative outcomes and the answers to these questions 159 are still discussed controversially in the scientific community. In a recent report on a   (Azam, 1998). It was estimated that bacteria could channel up to 50% 174 of marine primary production into the microbial loop, highlighting their importance in the 175 ocean's carbon cycle (Azam, 1998;Fenchel, 2008). Similarly, Legendre and Rivkin (2008) 176 found that heterotrophic microbes always dominate respiration in the euphotic zone, even 177 when most particulate primary production is grazed by metazoans. The ML intertwines with 178 the grazing food web and provides a mechanism to retain nutrients such as N and P in the 179 highly stratified upper oligotrophic oceans by recycling them through pico-phytoplankton, 180 bacteria and microzooplankton (Azam et al. 1983) (Fig. 2).

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The MCP complements and connects the concepts of BCP and ML, additionally including the 183 idea of the viral shunt, into a more integrated concept of the cycling of biogenic carbon in the 184 ocean. The viral shunt, which refers to the release of carbon and nutrients back into the 185 environment due to cell lysis, is tightly connected to the BCP, the ML and the MCP because 186 cell lysis transforms living particulate organic matter (POM) into DOM and non-living POM 187 (Wilhelm and Suttle 1999;Suttle, 2005). As much as a quarter of the C fixed by phytoplankton 188 is estimated to flow through the VS (Wilhelm and Suttle, 1999), thereby promoting ecosystem 189 respiration (Fuhrman, 1999). The released DOM and POM are largely of bacterial origin, and 190 hence, relative to bacterial requirements (because of the carbon required for respiration) have directly couples the VS to the ML and MCP, and has been termed the 'shunt and pump' (Suttle,197 2007).

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The BCP, ML and MCP have distinct ecological or biogeochemical meanings (Table 1), and 200 each has influenced multiple research disciplines (Table 2). These three concepts are 201 fundamental in developing global biogeochemical and ecological models that rely on 202 understanding organismal biology and the interactions between the POC and DOC pools (Fig.   203 3).    Here we focus on recent progress concerning the MCP in the context of the BCP and ML.  Table 3). The state of the art of these topics 228 will be discussed in the remainder of this review.     (Table 4).  (Table 4).

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The greater ages of lipid-like material than carbohydrate-and protein-like substances were  (Table 4). ); however, once the organisms die, their core lipids may be incorporated into larger 324 particles (0.7-to 60-m size fraction) that can be more quickly transported into the deeper 325 ocean and buried in marine sediments (Table 4). The same mechanism may apply to bacterial 326 lipid accumulation in the POM fraction that is preserved in marine sediments. It is unknown,  (Table 4). However, this pathway can be either biotic or abiotic and the 344 role that microorganisms play in the transformation of carotenoids to RDOM is unknown.   (Table 4).   It is well established that RDOM is composed of less than 10% of common biomolecules such 398 as carbohydrates, amino acids or lipids (see discussion above). Proxies such as the DOC:DON   (Table 4). I DEG was calculated using 10 mass peak magnitudes that       The interplay between bacterial community and DOM composition is also examined by

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The nutritional status of the environment may also affect the difference between  interaction at the ecosystem scale (Fig. 3). This is convincingly demonstrated by a long term   prevailing mechanism for carbon sequestration. In the case of a growing eddy, CE2 (modeling 630 scenario 2, Fig. 4), the rapid growth of phytoplankton caused enhancement of POC downward 631 export flux, where the BCP was the prevailing mechanism for carbon sequestration. Further 632 research is needed to validate these models for general applications.

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The second proposed approach is to strengthen the understanding of the connections between 677 microbial metabolism and the chemical structure of DOC compounds (e.g., Zhang et al., 2016).  We also highlight the need to examine the role of planktonic archaea in the carbon cycle.