Lessons from the genome of a lithoautotroph: making biomass from almost nothing.

Abstract

Most bacteria use organic carbon compounds from which they make their own cellular components. They derive energy from the exergonic catabolic reactions of these organic substrates and are known as “heterotrophs.” Autotrophs, in contrast, are able to use carbon dioxide as their sole source of carbon. The energy they require to do this may be obtained from the sunlight, e.g., in photosynthetic autotrophs, or from exergonic inorganic oxidation, as in chemolithotrophs. Nitrosomonas spp. derive all of their energy and reducing power for growth from the oxidation of ammonium to nitrite. These microorganisms require CO2, ammonium, and mineral salts for growth and manage to build a complex microorganism from “almost nothing.” This surprised me when I was an undergraduate student, and I was surprised again by the article by Chain et al. in this issue of the Journal of Bacteriology (2). The authors report that the genome of this microorganism is relatively small (fewer than 3 Mbp) and that all cell components are built with fewer than 2,500 proteins. Making biomass from “almost nothing” in Nitrosomonas europaea results in a relatively low growth rate. This microorganism's commitment to brevity is reflected by the presence of a single rRNA operon, which contrasts with faster-growing heterotrophs, which contain several copies (1, 5). Living on almost nothing forces the genes for the oxidation of ammonium (amo and hao) to duplicate, and this brings with it the duplication of certain cytochromes involved in electron transfer for energy gain (2). Apart from these examples no other genes are duplicated. N. europaea exhibits a large battery of cytochromes that make the cell highly dependent on iron acquisition. To guarantee adequate iron uptake, the genome sequence reveals one of the most striking findings: although the strain is only able to synthesize one iron-scavenging siderophore, it contains enough information for up to 20 different iron-receptor siderophores. Each iron receptor is linked to a pair of genes homologous to fecI-fecR, which are involved in sensing different iron siderophores and promoting transcription of the most appropriate uptake system (4). It would then seem that N. europaea has developed mechanisms to “steal” the iron captured by siderophores produced by other bacteria. This can be interpreted as an energy-saving system and as an opportunistic mechanism to colonize different niches. N. europaea seems to produce a large protein with Ca2+-binding domains that is highly similar to hemolysines. A similar protein has been described in Pseudomonas putida (3) and Pseudomonas fluorescens (S. M. Hinga, M. Espinosa-Urgel, J. L. Ramos, and G. A. O'Toole, unpublished data). Mutants deficient in the synthesis of this large protein in Pseudomonas spp. are impaired in surface attachment; thus, the protein might be involved in the early steps of biofilm formation (3; Hinga et al., unpublished). N. europaea also forms biofilms in which cell density seems to be controlled by quorum-sensing systems, although no definitive evidence for this is yet available. Almost 80% of the translated open reading frames of N. europaea matched sequences deposited in data banks, and of these sequences almost 87% had a known function. In other words, a potential function has been assigned to 70% of the all of the proteins produced by this microorganism. This allowed Chain et al. (2) to visualize biosynthetic pathways for essential cell components, such as the biosynthesis of nucleotides, amino acids, and fatty acids and to identify key elements in translation, transcription, and other processes. In accordance with the limited use of organic compounds is the fact that the genome sequence revealed few catabolic genes and few uptake systems for organic compounds. However, uptake systems for inorganic compounds or chemosensor systems to direct cells toward “appetizing” mineral sources were well represented. The unrestricted length of Journal of Bacteriology articles has enabled Chain and coauthors to offer readers a study rich in detail (2). In short, Chain et al. (2) have explained how a complex system (a microbe) can be made from very simple inorganic components and how N. europaea can interact with its environment. A number of questions remain open. Which signals turn on and off the limited set of genes of this chemolitotroph? What are the molecular details of intra- and intergenic communication with other players in their environment?