The obligate autotroph — the demise of a concept

Autotrophy is a life style in which inorganic compounds provide for all nutritional needs of an organism. Implicit in this definition is the capacity of an organism to derive all cell carbon from CO₂ and to obtain ATP either photosynthetically or chemolithotrophically. The existence of bacteria with such potentials has been known since the work of Winogradsky in the 1880's. The question explored in this paper is whether bacteria exist that must of necessity live autotrophically, i.e., the obligate autotrophsensu Winogradsky. The evidence is briefly reviewed and leads to four conclusions. One: there is no obligatory coupling between phototrophy and autotrophy or between chemolithotrophy and autotrophy. Two: autotrophic bacteria are not uniquely inhibited by organic matter. Three: all putative obligate autotrophic bacteria so far tested assimilate and metabolize exogenously supplied organic compounds. Four: mixotrophy can exist with respect to autotrophic and heterotrophic biosynthetic mechanisms and/or to chemolithotrophic and chemoorganotrophic energy-generating processes. Examples remain of bacteria that have not been cultured in the absence of an inorganic energy source or light. Such forms are appropriately described as obligate chemolithotrophs or obligate phototrophs. The available evidence, briefly categorized above, suggest that none of these bacteria is, at the same time, an obligate autotroph. From ecological and evolutionary considerations, an absolute dependence on carbon dioxide for all carbon makes little sense, and bacteria with such a requirement would be an anachronism on earth as it now exists. A lecture delivered before the third meeting of the Northwest European Microbiological Group, on August 18, 1971 at Utrecht, the Netherlands. The work reported from the author's laboratory was supported by grants from the National Science Foundation.