Elemental economy: microbial strategies for optimizing growth in the face of nutrient limitation.
Microorganisms play a dominant role in the biogeochemical cycling of nutrients. They are rightly praised for their facility for fixing both carbon and nitrogen into organic matter, and microbial driven processes have tangibly altered the chemical composition of the biosphere and its surrounding atmosphere. Despite their prodigious capacity for molecular transformations, microorganisms are powerless in the face of the immutability of the elements. Limitations for specific elements, either fleeting or persisting over eons, have left an indelible trace on microbial genomes, physiology, and their very atomic composition. We here review the impact of elemental limitation on microbes, with a focus on selected genetic model systems and representative microbes from the ocean ecosystem. Evolutionary adaptations that enhance growth in the face of persistent or recurrent elemental limitations are evident from genome and proteome analyses. These range from the extreme (such as dispensing with a requirement for a hard to obtain element) to the extremely subtle (changes in protein amino acid sequences that slightly, but significantly, reduce cellular carbon, nitrogen, or sulfur demand). One near-universal adaptation is the development of sophisticated acclimation programs by which cells adjust their chemical composition in response to a changing environment. When specific elements become limiting, acclimation typically begins with an increased commitment to acquisition and a concomitant mobilization of stored resources. If elemental limitation persists, the cell implements austerity measures including elemental sparing and elemental recycling. Insights into these fundamental cellular properties have emerged from studies at many different levels, including ecology, biological oceanography, biogeochemistry, molecular genetics, genomics, and microbial physiology. Here, we present a synthesis of these diverse studies and attempt to discern some overarching themes.
Department of Chemistry and Biochemistry, Institute for Genomics and Proteomics, University of California, Los Angeles, CA, USA.
Sabeeha S
SS
Merchant
John D
JD
Helmann
D000220:Adaptation, Biological; D018407:Bacterial Physiological Phenomena; D001711:Biotransformation; D002244:Carbon / Q000378:metabolism*; D002468:Cell Physiological Phenomena; D004734:Energy Metabolism; D019143:Evolution, Molecular; D053858:Metabolic Networks and Pathways / Q000235:genetics; D008670:Metals / Q000378:metabolism*; D009584:Nitrogen / Q000378:metabolism*; D010758:Phosphorus / Q000378:metabolism; D012623:Seawater / Q000382:microbiology*; D013455:Sulfur / Q000378:metabolism
D008670:Metals; D010758:Phosphorus; D013455:Sulfur; D002244:Carbon; D009584:Nitrogen