FEMS Microbiology Letters 112 (1993) 1-6
© 1993 Federation of European Microbiological Societies 0378-1097/93/$06.00
Published by Elsevier
FEMSLE 05559
MiniReview
Photosynthetic and quasi-photosynthetic bacteria
Howard Gest
Photosynthetic Bacteria Group, Department of Biology, Indiana University, Bloomington, Indiana, USA
(Received 18 March 1993; revision received 16 April 1993; accepted 11 May 1993)
Abstract: The term photosynthesis was coined in 1893 to represent the light-dependent conversion of
C O 2 and water to organic
compounds and molecular oxygen. Despite the discovery in 1907 that bacteriochlorophyll-containing purple bacteria do not
produce molecular oxygen and can grow on organic carbon sources using light as the energy source, photosynthesis is still
frequently defined as an oxygenic autotrophic process. The meanings of the terms photosynthesis and phototrophy have become
increasingly obfuscated, especially by the recent isolation of a number of aerobic bacterial species which produce bacteriochlorophyll but appear unable to use light as an energy source for appreciable biosynthesis. This paper focuses on the importance of
formulating a more precise definition of photosynthesis, and thereby forces recognition of the existence of a class of 'quasi-photosynthetic' bacterial species whose bioenergetic patterns require further analysis.
Key words: Bacterial photosynthesis; Phototrophy; Photoheterotrophy; Bacteriochlorophyll; Quasi-photosynthetic bacteria
Earlier definitions of photosynthesis
Following pioneering researches on plants in
the 18th century [1], the term photosynthesis was
proposed by C.R. Barnes in 1893 [2] to identify
the major plant process by which CO2 and water
are converted to sugars and molecular oxygen.
Barnes was led to coin the term because he
believed that previously used terms such as 'assimilation of carbon' or 'assimilation proper' could
be confused with similar terms in use for describing physiological processes in animals. In 1907,
Correspondence to: H. Gest, Photosynthetic Bacteria Group,
Department of Biology, Indiana University, Bloomington, IN
47405, USA.
Hans Molisch [3,4] demonstrated that so-called
non-sulfur purple bacteria do not produce 0 2
and also have the capacity to use organic compounds as carbon sources for growth with energy
provided by light. The latter photosynthetic
growth mode is now known as photoheterotrophy. In 1907, the properties of the non-sulfur
purple bacteria obviously did not satisfy the criteria for photosynthesis as originally defined for
green plants, and as a consequence, for several
decades the organisms were generally not accepted as being photosynthetic. Despite the fact
that during the past half century a large body .of
research has conclusively shown that anoxygenic
photoheterotrophy is a common growth mode for
many kinds of photosynthetic bacteria, definitions
of the term photosynthesis currently found in
many texts, dictionaries, and encyclopedias continue to describe only the oxygenic, autotrophic
green plant process.
The term phototrophy was redefined at a 1946
Cold Spring Harbor meeting of investigators [5],
who adopted a system of nomenclature for diverse organisms based on nutritional characteristics, i.e. on requirements for growth. Phototrophy
was proposed to apply to organisms able to obtain energy for growth 'chiefly' from photochemical reactions (whatever the carbon source). The
terms phototrophic and photosynthetic are now
being used interchangeably. To distinguish photosynthetic metabolic patterns in respect to carbon
sources for growth, the preferred terms are photoautotrophic for growth on carbon dioxide and
photoheterotrophic when the carbon source is an
organic compound(s).
Revised definitions of photosynthesis
In 1963, Kamen [6] suggested a revised definition of photosynthesis which would have the effect of including anoxygenic photosynthetic bacteria by (a) avoiding any specification of the carbon
source for growth, and (b) not indicating 0 2 as a
photosynthetic product. Kamen's definition:
"Photosynthesis is a series of processes in which
electromagnetic energy is converted to chemical
free energy which can be used for biosynthesis".
Kamen recognized that he had offered a "rather
noncommittal definition", and in fact it does not
convey the essential character of the phototrophic life mode. For reasons to be detailed
below, I propose the following provisional modification of Kamen's definition: Photosynthesis is a
series of processes in which electromagnetic energy is converted to chemical energy used for
biosynthesis of organic cell materials; a photosynthetic organism is one in which a major fraction
of the energy required for cellular syntheses is
supplied by light.
• What constitutes 'a major fraction' is obviously
arguable, and this aspect of the definition will no
doubt have to be discussed in the future depending on the results of research yet to be done on
organisms now being described as 'aerobic photo-
synthetic bacteria'. The revised definition proposed continues to reflect the fact that for 100
years, the essence of photosynthesis has been
understood as biomass production with light as
the energy source for biosynthesis.
Quasi-photosynthetic bacteria
During the recent past, a number of physiologically diverse aerobic bacterial species have been
described which produce bacteriochlorophyll a
(Bchl) but which appear in most instances to be
incapable of using light as a sole, major, or even
partial source of energy for growth. The increasing practice of referring to such organisms as
'aerobic photosynthetic bacteria' or as being
'photosynthetic' or 'phototrophic' is a corruption
of nomenclature bound to cause confusion in the
future.
The bacteria in question have been assigned to
various genera, including: Erythrobacter, Ery-
thromicrobium, Methylobacterium, Protaminobacter, Protomonas, Pseudomonas, Rhizobium,
Roseobacter, and Roseococcus. I suggest that for
the time being, organisms in these (and other)
genera which contain Bchl but are unable to use
light as the energy source for growth should be
described as quasi-photosynthetic. The marked
physiological differences between photosynthetic
and quasi-photosynthetic bacteria is perhaps best
illustrated by comparing 'profiles' of the two types
of organisms, using typical non-sulfur purple bacteria as the photosynthetic reference.
Non-sulfur purple photosynthetic bacteria
Energy for growth may be obtained in several
alternative ways. Optimal growth and maximal
Bchl synthesis are observed under anaerobic conditions with light (continuous illumination) as the
energy source• With rare exception, these organisms can also grow as aerobic heterotrophs in
darkness. Some species have the additional capacity to grow anaerobically in the dark with
energy provided by fermentation of sugars when
special 'accessory oxidants' are provided and under these conditions Bchl synthesis is abundant
[7]. In typical species, the presence of 0 2 strongly
represses synthesis of Bchl (and of 'photosynthetic reaction centers') [8]. The only known
species in which the regulatory effect of 0 2 o n
Bchl synthesis is greatly attenuated are Rhodospirillum centenum [9] and Rhodobacter sulfidophilus ([10]; the latter bacterium was formerly
known as Rhodopseudomonas sulfidophila). All
species grow well in the anaerobic photoheterotrophic mode and many can also grow photoautotrophically.
Quasi-photosynthetic bacteria
These organisms are heterotrophic aerobes.
Light does not serve as an energy source for
anaerobic growth. Some reports indicate that illumination improves aerobic growth, but few give
experimental documentation (see later). The
amount of Bchl produced (per mg dry weight) is
ordinarily quite low as compared with typical
non-sulfur purple bacteria grown photosynthetically [11]. Synthesis of Bchl is said to be suppressed when cultures are continuously illuminated (see Table 1). Since 0 2 is required for
growth (see, however, footnote a to Table 1) it is
not surprising that an 02-requirement for synthesis of Bchl is frequently reported. In regard to
carbon nutrition, the quasi-photosynthetic bacteria are diverse, ranging from methylotrophs to
ordinary heterotrophs.
From the foregoing profiles and comments in
Table 1, it is evident that there are great differences between photosynthetic and quasi-photosynthetic bacteria in respect to regulatory control
of Bchl synthesis and the significance of photosynthetic energy conversion in the normal physiology of the two groups of organisms. It appears
that a subgroup of quasi-photosynthetic bacteria
is chimeric in the sense that the bacteria can
grow using energy derived from both aerobic respiration and Bchl-based photophosphorylation.
Thus, an O2-dependent stimulation of growth by
light has been observed with a species of Erythrobacter [20]. Demonstration of the light effect
requires a preliminary phase of aerobic growth in
darkness. Similarly, Yurkov and van Gemerden
[21] have recently provided evidence that the
obligately aerobic bacterium Erythromicrobium
hydrolyticum can use light as a supplementary
Table 1
Bacteriochlorophyll synthesis in some quasi-photosynthetic bacteria
Organism
Observations
Erythrobacter longus OCh 114 a
Limitation of 0 2 results in decreased synthesis of Bchl; 0 2 stimulates Bchl production in
cultures previously grown semi-aerobically [12]
Porphyrobacter neustonensis
Synthesizes Bchl on 'low-nutrient media' under aerobic and semi-aerobic conditions;
production of the pigment 'was repressed on richer media such as casitone-yeast extract
agar' [13]
Protaminobacter ruber
Bchl content negligible in cultures grown in continuous light; Bchl production stimulated
by incubation in intermittent light [14]
'Pseudomonas extorquens'
Bchl not formed in illuminated cultures; Bchl produced in darkness and in a light/dark
regimen [15]
TK 0001
Rhizobium strain BTAi 1
'Pigment formation in liquid cultures of BTAi 1 was observed only with intermittent
lighting; under continuous illumination or continuous darkness no pigmentation was
found' [16]
Roseococcus thiosulfatophilus b
Cells of this aerobic 'chemoorganotrophic' species contain Bcbl; the species is said to be
'facultatively photoheterotrophic,' but it is also stated that the organism does not grow
anaerobically in the light [17]
a
Erythrobacter sp. strain OCh 114 (ATCC 33942), also known as Roseobacter denitrificans [18], has the capacity to grow
anaerobically in darkness with nitrate as the terminal electron acceptor; Bchl synthesis is severely inhibited under these growth
conditions and light has no effect on the rate of anaerobic growth or denitrification [19].
b Some species of Roseococcus were formerly classified in the genus Erythrobacter.
energy source for growth under certain circumstances. Professor Michael Madigan (Southern
Illinois University) has suggested to me that E.
hydrolyticum and similar organisms could be designated as paraphotosynthetic in view of the dictionary meaning of para- as "in an accessory or
secondary capacity".
The special case of Halobacterium
The description of bacteria in the genus
Halobacterium as photosynthetic or phototrophic
is a misnomer. Under conditions of diminished
pO2, these aerobic bacteria produce pigmented
membranes capable of photophosphorylation, i.e.
light-dependent regeneration of adenosine triphosphate from adenosine diphosphate and inorganic phosphate. However, the halobacteria do
not contain chlorophyll or bacteriochlorophyll and
as far as is known their photophosphorylation
process does not involve electron transport and
redox reactions of the kind associated with genuine photosynthetic energy conversion. Moreover, it is not established that the photophosphorylation capacity demonstrable with Halobacterium membrane preparations in vitro can support continuous light-dependent cell growth as in
true photosynthesis. Experimental data [22,23]
purported to demonstrate anaerobic light-dependent growth of halobacteria under special nutritional conditions indicate very slow, limited
growth of only one to two doublings with atypical
kinetics (linear, rather than logarithmic). Stoeckenius [24] has noted: "We have been unable to
obtain continuous [my italics] growth of H. halobium under strictly anaerobic conditions in either
complex or simple media." It seems likely that
Halobacterium will prove to fall in the paraphotosynthetic category of bioenergetic patterns.
Closing remarks
It may transpire that further research will show
that under appropriate growth conditions some
quasi-photosynthetic bacteria are indeed photosynthetic according to the most accepted understanding of the terms under discussion. It is conceivable, however, that the presence of relatively
small amounts of the photopigments in quasiphotosynthetic organisms does not necessarily reflect a potentiality for the massive energy conversion (or energy storage) characteristic of photosynthesis.
J.S. Fruton [25] recently commented on problems relating to the improvement of scientific
nomenclature: "These problems have not been,
as some biologists, chemists, or biochemists may
have believed, trivial concerns of pedantic editors
of scientific journals, but have reflected the state
of the development of an area of inquiry at a
particular time. I believe, therefore, that an application of the changes in the language used
within a research discipline is essential for the
understanding of the development of the conceptual framework of that discipline."
Improving the nomenclature of bioenergetic
types of bacteria influenced by light provides a
focus on unsolved physiological, biochemical, and
evolutionary problems of interest. Why are
quasi-photosynthetic bacteria unable to couple
photochemical energy conversion to biosynthesis
of cell materials? Have certain quasi-photosynthetic bacteria acquired Bchl synthesis genes by
lateral gene transfer? Does the capacity of quasiphotosynthetic bacteria to synthesize Bchl merely
reflect the evolutionary loss of other genes required for photosynthesis from photosynthetically-competent ancestors? These questions, and
others, arise from recognition of quasi-photosynthetic bacteria as a group of organisms distinct
from bacteria that are genuinely photosynthetic.
Acknowledgement
Research of the author on photosynthetic bacteria is supported by National Science Foundation Grant DCB-8915037.
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