The evolution of inorganic carbon concentrating mechanisms in photosynthesis

Abstract

Inorganic carbon concentrating mechanisms (CCMs) catalyse the accumulation of CO 2 around rubisco in all cyanobacteria, most algae and aquatic plants and in C 4 and crassulacean acid metabolism (CAM) vascular plants. CCMs are polyphyletic (more than one evolutionary origin) and involve active transport of HCO K 3 , CO 2 and/or H C , or an energized biochemical mechanism as in C 4 and CAM plants. While the CCM in almost all C 4 plants and many CAM plants is constitutive, many CCMs show acclimatory responses to variations in the supply of not only CO 2 but also photosynthetically active radiation, nitrogen, phosphorus and iron. The evolution of CCMs is generally considered in the context of decreased CO 2 availability, with only a secondary role for increasing O 2 . However, the earliest CCMs may have evolved in oxygenic cyanobacteria before the atmosphere became oxygenated in stromatolites with diffusion barriers around the cells related to UV screening. This would decrease CO 2 availability to cells and increase the O 2 concentration within them, inhibiting rubisco and generating reactive oxygen species, including O 3 .

To concentrate or ventilate? Carbon acquisition, isotope discrimination and physiological ecology of early land plant life forms

“…for the pyrenoid in Chlamydomonas and other algal lineages. While there are undoubtedly some CCM systems which function in the absence of a pyrenoid (Raven 1997a,b;Raven et al 2008), we contend that the majority of the significant aquatic global carbon fixation mediated by noncyanobacterial microbes (Raven et al 2008) is mediated by a pyrenoid-based CCM. To date, there are no candidate genes, proteins or specific structures which are thought to comprise a pyrenoid, other than the associated starch sheath (Izumo et al 2007), and internal pyrenoid complement of rubisco (Lacoste-Royal & Gibbs 1987;Vaughn et al 1990;Borkhsenious et al 1998), rubisco activase (McKay et al 1991), nitrate reductase (Okabe & Okada 1990), Calvin cycle enzymes, photosystem I and lumenal carbonic anhydrase-enriched trans-thylakoid lamellae (Villarejo et al 1998;Moroney & Ynalvez 2007).…”

“…These data are again consistent with the role of the CCM in non-ventilated hornworts as providing equivalence, in terms of carbon gain, to that of ventilated thalli (Hanson et al 2002;Griffiths et al 2004). However, the CCM rates would be a disadvantage in terms of the energetic demand in a low light environment, again leading to the conclusion that there was possibly little long-term physiological advantage in retaining a CCM for the early evolution of land plants in a high CO 2 world in shaded habitats (Griffiths et al 2004;Raven et al 2008).…”

Carbon dioxide mitigation potential of seaweed aquaculture beds (SABs)

“…It has been estimated that seagrasses, saltmarshes, and mangroves can capture 70% of C in the marine area (Nelleman et al 2009. Seaweeds utilize inorganic carbon dissolved in seawater as free CO 2 that diffuses in through cellular membranes from the surrounding seawater (Turan and Neori 2011) and as bicarbonate that is actively pumped into the cell via a carbon concentrating mechanism (Giordano et al 2005;Raven et al 2008). Moreover, the transformation by seaweeds of DIC into organic carbon by photosynthesis can decrease the pCO 2 in seawater (Tang et al 2011).…”

AFestschriftin honour of Professor John A. Raven

“…Despite the apparent excess of inorganic carbon relative to available nitrogen, phosphorus and iron in surface seawater (Raven et al 2005b;Falkowski and Raven 2007), the speciation of inorganic carbon in seawater and the kinetics of the core carboxylase ribulose bisphosphate carboxylaseoxygenase, explain the almost universal occurrence of inorganic CCMs in marine phytoplankton (Giordano et al 2005). Recent work has investigated the phylogenetic distribution of the various CCMs (Giordano et al 2005;Raven et al 2008), how their expression is influenced by the availability of other resources (Giordano et al 2005;Raven et al 2005b), and how some phytoplankton organisms can manage without CCMs (Giordano et al 2005;Raven et al 2005c). This work is continuing, with emphasis on responses to the changes in surface ocean chemistry attendant on increasing anthropogenic inputs of CO 2 to the atmosphere and hence to the surface ocean (Raven et al 2008).…”

“…Recent work has investigated the phylogenetic distribution of the various CCMs (Giordano et al 2005;Raven et al 2008), how their expression is influenced by the availability of other resources (Giordano et al 2005;Raven et al 2005b), and how some phytoplankton organisms can manage without CCMs (Giordano et al 2005;Raven et al 2005c). This work is continuing, with emphasis on responses to the changes in surface ocean chemistry attendant on increasing anthropogenic inputs of CO 2 to the atmosphere and hence to the surface ocean (Raven et al 2008).…”