Chapter 2

Photooxidation of Mn-bicarbonate Complexes by Reaction Centers of Purple Bacteria as a Possible Stage in the Evolutionary Origin of the Water-Oxidizing Complex of Photosystem II

Vasily V. Terentyev*, Andrey A. Khorobrykh, Vyacheslav V. Klimov

Institute of Basic Biological Problems, Russian Academy of Science, Institutskaya Street 2, Pushchino, Moscow Region, 142290, Russia

*Corresponding author: v.v.terentyev@gmail.com

Abstract

In recent years significant progress in the study of the structural and functional organization of the Mn-cluster (inorganic core) of the water-oxidizing complex (WOC) of photosystem II (PS II) has been achieved. Despite this fact, the question about the evolutionary origin of the inorganic core of the WOC of PS II still remains open. The results of electrochemical and EPR measurements show that in the presence of bicarbonate ions, the oxidation of Mn2+ cations is significantly facilitated upon formation of Mn2+-bicarbonate complexes. The oxidation potential of Mn2+ to Mn3+ in the Mn2+-bicarbonate complex is low enough, that the photooxidation of Mn2+ by reaction centers (RCs) of anoxygenic photosynthetic bacteria could be expected. Based on this, an assumption about a possible role of the "low-potential" Mn2+-bicarbonate complexes in the evolutionary origin of the Mn-cluster of the WOC of PS II was made. Such complexes could be used by anoxygenic bacteria containing type II RCs initially as electron donors, and then as "building blocks" for the formation of the enzymatic Mn-containing center capable to do the water oxidation that could lead to the appearance of the first O2-evolving cyanobacteria. This chapter describes current research in this area.

Keywords: Mn-bicarbonate complexes, purple bacteria, photosynthetic reaction centers, evolution of photosynthesis

2.1 Introduction

Appearance of oxygenic photosynthetic organisms more than 2.5 billion years ago led to the accumulation of O2 in Earth's atmosphere, dramatic reorganization of the biosphere and the beginning of aerobic life (Holland and Rye, 1998; Des Marais, 2000; Dismukes and Blankenship, 2005).

The formation of photosynthetic molecular oxygen takes place within the multiple enzymatic water oxidizing complex (WOC) of photosystem II (PS II) of plants and cyanobacteria as a result of four-electron oxidation of two water molecules (see Renger, 2001). The basis of the WOC is a so-called inorganic core (Mn-cluster) composed of four atoms of Mn, one atom of Ca and five atoms of O (Umena et al., 2011).

Reaction centers (RCs) of purple bacteria related to type II RC (pheophytin-quinone type) are the most favorable evolutionary precursors for PS II (Blankenship, 1992; Allen and Williams, 1998; Allen, 2005). In spite of this, the evolutionary transition of anoxygenic photosynthesis to oxygenic one is under debate up to this day.

The redox potential of the P+/P pair in RC containing bacteriochlorophyll is about 0.5 V (Lin et al., 1994), which is enough for oxidation of iron, some organic and sulfide compounds etc. which are used by anoxygenic photoautotrophs as electron donors, but it is not enough for manganese oxidation.

The hypothesis about a possible role of the Mn2+-bicarbonate complexes in the evolutionary origin of the Mn-cluster of the WOC is currently under development (Dismukes et al., 2001; Kozlov et al., 2004; Dasgupta et al., 2006). Electrochemical and EPR measurements have shown that the oxidation of Mn2+ becomes easier in the presence of bicarbonate ions (Kozlov et al., 2004; Dasgupta et al., 2006; Tikhonov et al., 2006). In this way, the potential of a one-electron oxidation of Mn2+ to Mn3+ shifts from 1.18 V (aqua-complex) to 0.61 V and 0.52 V under the formation of the complexes [Mn(HCO3)]+ and [Mn(HCO3)2], respectively. Formation of the "low-potential" Mn2+-bicarbonate complexes like these facilitates the photooxidation of Mn2+ during the process of photoinduced assembly of the inorganic core of the WOC (Klimov et al., 1995a, 1995b; 1997a; Allakhverdiev et al., 1997; Baranov et al., 2000; Baranov et al., 2004; Kozlov et al., 2004). In addition, the oxidation potential of the Mn2+ -bicarbonate complexes becomes so low (about 0.52 V) that Mn2+ can be oxidized by even RCs of anoxygenic photosynthetic bacteria. Therefore, it has been suggested that such complexes could be used by anoxygenic bacteria as electron donors and as "building blocks" in the time of formation of the first O2-evolving photosynthetic RCs (Dismukes et al., 2001; Kozlov et al., 2004; Dasgupta et al., 2006).

2.2 Appearance of Photosynthesis

According to modern concepts, photosynthetic organisms were one of the first life forms on Earth (Blankenship, 1992; Braiser et al., 2002; Olson and Blankenship, 2004; Dismukes and Blankenship, 2005; Rashby et al., 2007).

The emergence of anoxygenic phototrophic metabolism apparently occurred immediately after the chemosynthetic metabolism, and in the early Archaean era it gained the widest spread because restorative substrates (such as Fe2+, S2-, and others) and CO2 were in excess (Holland and Rye, 1998; Des Marais, 2000; Dismukes and Blankenship, 2005).

Many facts have been presented as evidence in favor of the early occurrence of phototrophic metabolism. For example, the date of the appearance of photosynthetic microorganisms (about 3.5 - 3.7 billion years ago), determined by a comparative study of 16S ribosomal RNA (rRNA) (the method "molecular clock"), agrees well with the time of origin of the most ancient stromatolites recognized by many researchers as fossils of cyanobacterial mats (Awramik, 1992; Buick, 1992; Schopf et al., 2007). However, it is easy to confuse them with filamentous anoxygenic bacteria of the evolutionary ancient group Cloroflexi, which is morphologically indistinguishable from cyanobacteria.

In consideration of the anaerobic conditions of the atmosphere and hydrosphere in that time, we could not exclude the possibility that the earliest bacterial mats were formed not by cyanobacteria, but filamentous phototrophic bacteria with the participation of unicellular purple and green sulfur bacteria.

The data of isotopic studies concerning autotrophic carbon fixation (the effect of fractionation of stable isotopes C12/C13 accompanying photosynthesis) shift that date closer to 3.8 billion years ago (Schidlowski, 1988; Schopf et al., 2007), and, in turn, suggest that the organisms, whose remains are stromatolites, were photosynthetic one.

Thus, according to published data, photosynthetic organisms appeared 3.5 - 3.8 billion years ago. Oxygenic photosynthesis arose much later.

It is generally accepted that oxygenic photoautotrophs (cyanobacteria) appeared 2.5 - 2.7 billion years ago. The remains of cyanobacteria were described in the province of Transvaal in South Africa and in the older strata series Fortescue in Western Australia. Organic rocks from Pilbara (Australia), which are approximately 2.7 billion years old, preserve biomarkers of cyanobacteria - 2-methlhopanoids (Summons, 1999). Molecular oxygen began to accumulate in the atmosphere 2.3 - 2.2 billion years ago (Buick, 1992; Holland and Rye, 1998) and most likely it was of photosynthetic origin (Holland and Rye, 1998; Farquhar et al., 2000; Kasting and Seifert, 2002).

Modern cyanobacteria are the simplest of oxygen-evolving organisms. Nevertheless, the organization of their photosynthetic apparatus has quite strong similarities with higher plants.

No primitive oxygenic bacterium that could be an evolutionary precursor of cyanobacteria has yet been found.

2.3 Classification of Photosynthetic Bacteria

The process of photosynthesis, in prokaryotes and eukaryotes reveals striking similarities which gives every reason to believe that all (bacterio-)chlorophyll-containing photosynthetic organisms evolved from a common photosynthetic ancestor.

Anoxygenic photosynthetic organisms are exclusively prokaryotes, and traditionally they are classified into families based on their phenotype, contained pigments and metabolic features (Pfenning and Trüper, 1983; Imhoff, 1995; Madigan and Ormerod, 1995; Pierson and Castenholz, 1995; Gemerden and Mas, 1995). However, there is another classification system now fairly widely accepted. It is based on a comparison of the sequences of 16S rRNA, resulting in a division of all living organisms into three genealogical clusters (domains): Archeae, Bacteria and Eucarya (Woese, 1987). As a result, all photosynthetic bacteria belong to the domain Bacteria (Figure 2.1), within which the capacity for phototrophy is known for representatives only from six very mutually distant phylogenetic branches: Cyanobacteria, Proteobacteria (Purple bacteria), Chlorobi, Firmicutes, Chloroflexi and Acidobacteria. Chloroplasts belong to cyanobacteria and most probably entered into the eukaryotic cell by endosymbiosis (Gray, 1989). The only representative of the poorly studied phylogenetic branch Acidobacteria is the recently isolated photosynthetic bacteria Chloracidobacterium thermophilum (Bryant et al., 2007).

Figure 2.1 Evolutionary tree of life based on small subunit rRNA analysis. Taxa that contain photosynthetic representatives are highlighted in color, with...