Bulletin du Centre Franco-Japonais d'Histoire des Sciences (Kitakyushu-Paris), Vol. 14(2): 9-20 (2020)
日仏科学史資料センター紀要

ISSN 1882-3548 (online), 1882-353X (CD-ROM)-Mini ReviewScientific history of cyanobacteria research: Achievements of Roger
Stanier (1916-1982) and the mechanisms of inorganic carbon
enrichment in cyanobacteria.*
Hiroshi Ohkawa1,2
12Faculty of Agriculture and Life Science, Hirosaki University, Hirosaki, Japan;

International Photosynthesis Industrialization Research Center, Faculty of Environmental Engineering,
The University of Kitakyushu, Kitakyushu 808-0135, Japan.

(hohkawa@hirosaki-u.ac.jp)

Abstract
Cyanobacteria (previously known as blue-green algae) are known for prototypic oxygenevolving photosynthesis functionming in the same manner as plants, appered on Earth ca. 3.8 billion
years ago, and they still survive and thrive today. In the history of science, cyanobactera have made agreat contributions to the development of photosynthesis research. In 1996, the entire nucleotide
sequence of the Pasteur collection strain Synechocystis sp. PCC6803 was determined for the first time
among the photosynthetic model organisms. Roger Stanier, who contributed to the Pasteur culturecollection of cyanobacteria, was a prominent microbiologist who laid the foundation forcyanobacterial research, including establishing the name Cyanobacteria. This paper briefly describes
the history of cyanobacterial research with emphasis to the works of Stanier and the mechanism of
inorganic carbon (Ci) enrichment due to which cyanobacterial photosynthesis is efficiently driven.

Keywords: CO2 concentrating mechanism, cyanobacteria, inorganic carbon (Ci), Institut
Pasteur, Pasteur culture collection (of cyanobacteria), Roger Stanier.

Ohkawa, H. (2020) Scientific history of cyanobacteria research: Achievement of Roger Stanier (19161982) and the mechanisms of inorganic carbon enrichment in cyanobacteria. Bull. Cent. Fran. Jpn. Hist.
Sci. 14(1): 9-20.

*This is a peer-reviewed article communicated by Prof. T. Kawano (Univ. Kitakyushu). Preliminarily
communicated for the concept of article in September, 2019; first complete manuscript received on
April 13th; 2020; Revised after comments by reviewers on April 13th, 2020; Accepted for publication
on April 14th, 2020.

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Introduction
Cyanobacteria are photosynthetic prokaryotes that have been photosynthetic for billions of years
on Earth. They have attracted scientists as model organisms for the study of plant biology involving
oxygen photosynthesis. While photosynthesis in cyanobacteria is governed by a single set of genomes,that found in higher plants is governed by genetic information encoded by both nucleic andchloroplastic genomes. Obviously, the size of the cyanobacterial genome is much smaller than that ofhigher plants. Cyanobacteria are also considered as one of potential ancenstors of chloroplasts.
Evidence has also been shown from the analysis of genomic information (Martin et al., 2002).
Therefore, it is an attractive organism as a chloroplast model not only for microbiologists but also forbotanists. In recent years, microalgae including cyanobacteria have gained much attention, because
they are important organisms for biotechnologies for producing food additives, bioactive substances,
pharmaceutical compounds, biofuels (Abed et al., 2009, Khetkorn et al., 2017). In traditionalclassifications, morphological distinctions have been used to divide the group into five subsections(Rippka et al. 1979). Recent phylogenic studies based on 16S rRNA have demonstrated further
diversity. Therefore, the discussion on their phylogeny as well as the current number of cyanobacterial
species are still controversial (Foster et al., 2009, Tomitani et al., 2006).
This short article presents a brief history of cyanobacterial research and short review of themechanisms of Ci enrichment in the cell.

Blue-green algae (cyanophyceae) or blue-green bacteria (cyanobacteria) ?
Cyanobacteria were originally called blue-green algae. The classical term was derived from alga
which looks blue-green by phycocyanin and chlorophyll a. For over a century, cyanobacteria havebeen considered to belong to the algal group. It was actually classified under the International
Botanical Naming Convention (now the International Algae, Fungi and Plant Naming Convention).
However, Stanier et al. (1978) has proposed the name cyanobacteria in the ICNP (the International
Code of Nomenclature of Prokaryotes), and is the term that has become the most established.
Table 1 compares the popularities of the scientific names/terms for this organism, namely
cyanobacteria, blue-green bacteria, cyanophyceae, and blue-green algae, to be used in the titles ofscientific publications (papers). Among four names, "blue-green algae" was oldest term given to thisorgamnism (Richards, 1901). In the early 1900s, "blue-green algae" was most friquently used termsuggesting its popularity among scientific community. Additionally, "cyanophyceae" was temporally
used in limited number of publications (tottaly 54) since the first appearance in the work by Lloyd in
101923. However, the term "cyanobacteria", which appeared half century later, was accepted and usedin 3648 articles and its overwhelmingly used today.
While the researchers started to use both “cyanobacteria” and “blue-green bacteria” in the 1970s,"cyanobacteria" has been largely favored by majority of the biologists who documented a number ofarticles throughout the decades since the first appearance of the termup to today. On the other hand, it
seems that "blue-green bacteria" did not penetrate into the research community. In the process that“cyanobacteria” gained the popularity ammong the scientific communities, Stanier's constantachievements might have been significant.
Table 1. Comparison of the number of papers using the the related terms (cyanobacteria, bluegreen bacteria, cyanophyceae or blue-green algae) in the titles.
number of articles
the terms

total number

year 2019

oldest article

cyanobacteria

3648

299

Lemasson, et al. (1973)

blue-green bacteria

210Ingram, et al. (1973)

cyanophyceae

541

Lloyd (1923)

blue-green algae

534

4Richards (1901)

The number of articles with each term was estimated based on the searches with PubMed database.

Roger Stanier and Pasteur culture collection of cyanobacteria
After contributing to the understanding of the microbial world (Stanier R., et al.,1962) at the University of California at Berkeley, Stanier, a world-renowned
microbiologist, moved to the Institute of Pasteur in France, where he achieved many
research achievements such as the classification of cyanobacteria, andalsophysiological and morphological studies of cyanobacteria (Kenyon et al., 1970, Stanier,
1971, Pelroy et al., 1972). The cyanobacterial collection at Berkeley (Berkeley strain) has
been preserved as the Pasteur culture collection of cyanobacteria (PCC strain) and has
contributed to the development of various studies to date.
For the first time as a photosynthetic organism, the entire nucleotide sequence of
cyanobacteria was decoded by the Kazusa DNA Research Institute (Kaneko et al., 1996).
The cyanobacterium used for this decoding is a unicellular spherical Synechocystis sp.
PCC6803 (Fig. 1A). The complete nucleotide sequence of unicellular Synechococcus

11elongatus PCC7942 (S. elongatus PCC6301 is the type strain for S. elongatus, Fig. 1B),
which was first reported as a strain capable of natural transformation, has been determined.
In this way, the Pasteur culture collection of cyanobacteria contributed by Stanier
et al. forms the basis of cyanobacterial research development to date by elucidating theshape and physiological characteristics of cyanobacteria that differ in classification andthe complete genome base sequence.

(A(B

Fig. 1. Microscopic photographs of two different cyanobacterial strains. (A) Syenchocystis sp.
PCC6803; (B) Synechococcus elongatus PCC7942. The scale bars represent 20 µm for both
microscopic panels (Olympus BX53, Tokyo)

Carbon fixing in photosynthetic organisms
Plants and other oxygen-generating photosynthetic organisms absorb CO2 and produce reducing
sugars through the Calvin cycle. Ribulose - 1,5 - bisphosphate carboxylase / oxygenase (Rubisco), theinitial carbon-fixing enzyme in the circuit, produces two molecules of 3-phosphoglycerate (3-PGA)
by a carboxylase reaction that fixes CO2. On the other hand, it also has oxygenase activity that reacts
with O2, producing 3-PGA and phosphoglycolic acid. Rubisco has a lower affinity for O2 than that of
CO2, but under current atmospheric conditions (21% O2, 0.04% CO2), the Rubisco oxygenase reaction
will always work due to the very high O2 concentration. This oxygenase reaction results in a loss of12

energy and organic carbon, reducing the efficiency of CO2 fixation. Therefore, it can be said that theaffinity of Rubisco for CO2 and O2 and the ratio of CO2 to O2 around Rubisco are the main factors
controlling the efficiency of photosynthesis.
However, to overcome these problems, cyanobacteria have a mechanism to increase the CO2 /O2 ratio around Rubisco and suppress photorespiration by concentrating Ci in cells (CO2 concentrating mechanism: CCM).

Cyanobacterial CCM
Plants and other oxygen-generating photosynthetic organisms absorb CO2 and produce reducing
sugars through the Calvin cycle. Ribulose - 1,5 - bisphosphate carboxylase / oxygenase (Rubisco), theinitial carbon-fixing enzyme in the circuit, produces two molecules of 3-phosphoglycerate (3-PGA)
by a carboxylase reaction that fixes CO2. On the other hand, it also has oxygenase activity that reacts
with O2, producing 3-PGA and phosphoglycolic acid. Rubisco has a lower affinity for O2 than that of
CO2, but under current atmospheric conditions (21% O2, 0.04% CO2), the Rubisco oxygenase reaction
will always work due to the very high O2 concentration. This oxygenase reaction results in a loss ofenergy and organic carbon, reducing the efficiency of CO2 fixation. Therefore, it can be said that theaffinity of Rubisco for CO2 and O2 and the ratio of CO2 to O2 around Rubisco are the main factors
controlling the efficiency of photosynthesis.

Physiological properties of CCM and isolation of HCR mutants:
To elucidate the cyanobacterial Ci transport system, physiological analysis has been performedon the Ci transport characteristics, and the main characteristics have been clarified. (1) Although it has
high affinity for CO2, it has low affinity for bicarbonate ions, about 1/100 of its affinity for CO2(Volokita et al., 1984). (2) The requirements for sodium are different (Espie GS. et al., 1988). A highconcentration of sodium ions (> 10 mM) is required for bicarbonate transport, whereas a low
concentration of sodium ions (> 0.1 mM) is sufficient for CO2 transport (Miller, AG. and Canvin DT.,
1985).

For these reasons, it has been thought that CO2 and bicarbonate ions are transported inseparate systems. (3) The ratio of Ci in cells is different. No matter which type of Ci is given,bicarbonate ions are selectively accumulated in the cells.
Subsequently, in order to elucidate these mechanisms at the molecular level, a number ofmutants requiring high CO2 (HCR) that required high concentrations of CO2 to grow were isolated,and many of the causative genes were carboxysomes and carbonic anhydrase (Friedberg et al., 1989,
Schwarz et al., 1992, Ogawa et al., 1987, Kaplan et al., 1991, Fukuzawa et al., 1991). Among them, amutant lacking the ability to transport CO2 was first isolated (Ogawa, 1990). This ushered in a13

molecular understanding of the Ci transport system. To date, five Ci transport pathways have been
identified for cyanobacteria.

Two CO2 transport routes:
From the analysis of the double mutants, NdhD1/2 is essential for photoheterotrophic and PSI
cyclic electron transfer, and NdhD3/4 is involved in CO2 uptake. The existence of 1 was suggested(Ohkawa et al., 2000). In addition, ndhD4 is constitutively expressed, ndhD3 gene is induced at low
CO2 concentration, and ndhF3, ndhD3 and cupA are co-transcribed, and all mutants show the same
phenotype as ndhD3 mutant Therefore, it was suggested that CupA is a constituent subunit of NDH-1
including the ndhD3 subunit (Ohkawa et al., 1998, Ohkawa et al., 2000). On the other hand, ndhF4,
ndhD4 and cupB mutants show low CO2-induced uptake characteristics (Shibata et al., 2001, Shibata
et al., 2002). In other words, high-affinity CO2 uptake via NDH-1 containing NdhD3, ndhF3 and cupA(later NDH-1MS or NDH-13) and NDH-1 containing ndhD4, ndhF4 and cupB (later NDH-1MS 'or
NDH-14).

Three HCO3- transport routes:
The transport of bicarbonate ion, another substrate, is a pathway that is taken up into cells bytransporters located in the cell membrane, but three types of transporters have been known so far.
BCT1 (Bicarbonate transporter) was first identified as a low CO2-inducible cell membrane protein
CmpA of Synechococcus 7942 (later, a substrate-binding subunit of BCT1) (Omata et al., 1986, Omata
et al., 1999). Subsequently, analysis using a constantly expressed strain proved physiologically the
first time to be a high-affinity bicarbonate ion transporter BCT1. Next, a sodium-dependent highaffinity bicarbonate ion transporter (SbtA) was isolated from Synechocystis 6803 (Shibata et al., 2002).
This is a low CO2 inducible type, and if the CO2 transport ability is deficient, it is essential in a low
CO2 growth environment at alkaline pH, and plays an important role in the acquisition of Ci in a CO2
restricted environment. The third transporter (BicA) is a sodium-dependent low-affinity transporter
isolated from the marine cyanobacterium Synechococcus PCC7002. It belongs to the SulP/SLC26
family, which is widely conserved from prokaryotes to eukaryotes, and BicA homologs exist in anygroup of cyanobacteria (Shelden et al., 2010).

Different Ci transport systems depending on carboxysome type:The evolutionary comparison of CCM has been made based on the comparison of various
cyanobacterial genome information. It has been proposed that cyanobacterial carboxysomes be
divided into two types based on the differences in the constituent Rubiscos (Badger et al., 2002). Those
having Form-1B Rubisco, ccm-type carboxysome (β-carboxysome) are β-cyanobacteria, and those of14

Form-1A Rubisco, cso-type carboxysome (α-carboxysome) are α-cyanobacteria. Comparing thenumbers of Ci transporters between these types, many freshwater β-cyanobacteria possess all five of
the above pathways (Fig. 2), while α-cyanobacteria have a number of Ci transport pathways. And thenumber is often missing or partially missing (Ogawa et al., 2007).

Fig. 2. Cyanobacterial CCM model. This figure shows a typical freshwater ß-cyanobacterial model.
There are five inorganic transport systems, namely, three types of HCO3- transporting systems and two
types of CO2 transport systems as shown in this figure. Note that α-cyanobacteria lack BCT1 andNDH-1MS.

Conclusion
This short review described the history of Cyanobacteria research. The study of Stanier and coworkers of the Institut Pasteur in France would be a great achievement to be commended for thetaxonomic status of cyanobacteria and the research-based cyanobacterial strain collection. In recent
years, attempts have been made to isolate microalgae including cyanobacteria, and various reports
have been made indicating that the microalgae have characteristic properties as compared with theirhomologous strains (Yu et al., 2015, Nitanai et al., 2015, Nguyen et al., 2017, Ohta et al., 2018,15

Konstantinou et al., 2018). It has been suggested that Ci transport is carried out by various pathways,
and that the transport pathway of Ci differs depending on the classification of carboxysome, which isa place for carbon fixation. More than 40 years after the initial research, the elucidation of
cyanobacterial CCM has greatly advanced.
As with Stanier's pioneering research approach, understanding the differences in morphological,
physiological, and chemical properties associated with various cyanobacteria will continue to be better
understood.

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シアノバクテリア研究の科学史： Roger Stanier（1916-1982）の功績とシアノ
バクテリアにおける無機炭素濃縮機構
要約
植物と同様に酸素発生型の光合成を行うシアノバクテリアは、光合成研究の発展に大きく貢献してきた生物材料である。 1996 年、光合成モデル生物として初めて、パスツールコレクション Synechocystis sp.
PCC6803 株の全ヌクレオチド配列が明らかにされた。このコレクションの「構築に貢献した Stanier は著
名な微生物学者であり、シアノバクテリアという用語の確立を含め、シアノバクテリアの研究の基礎を築いた。本論文では、Stanier の功績をはじめとしたシアノバクテリア研究の歴史と、シアノバクテリアの光合成において重要な役割を果たす無機炭素（Ci）濃縮のメカニズムについて簡単に解説する。

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