Elemental economy: microbial strategies for optimizing growth in the face of nutrient limitation - PubMed (original) (raw)

Review

Elemental economy: microbial strategies for optimizing growth in the face of nutrient limitation

Sabeeha S Merchant et al. Adv Microb Physiol. 2012.

Abstract

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.

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Figures

Figure 1

Mendeleev meets Darwin. Dmitri Mendeleev (1834–1907) (left) developed the periodic table of the elements (ca. 1869). Charles Darwin (1809–1882) (right) developed the theory of evolution by natural selection.

Figure 2

A cellular perspective on the periodic table. Essential macronutrients are in white against a black background and universally essential cations (Zn, Mg) in white against a grey background. Elements that have important biological roles in many but likely not all cells are shown in boldface against a dark grey background. These include the key transition metals (Mn, Fe, Co, Cu, Mo) and cations (K). Elements that are used for specialized purposes in some microbes are shown against a light grey background. These include a requirement for boron (B) in plants for cell wall structure and in some bacteria for quorum sensing. Elements that may have specialized uses, but are not known to contribute to growth are in large font against a white background (Cr,Cl, I).

Figure 3

Atomic composition of Synechococcus sp., a representative of the bacterial phytoplankton. For each pie chart, the portion indicated by the asterisk (other) is expanded in the pie chart to the right. On the far right, Sr is indicated by the black slice and the thin white slice between Cu and Sr includes Co and Cd. Plotted with data from (Quigg et al. 2011).

Figure 4

Overview of the biological roles of C and known sparing and recycling mechanisms (see text for details.)

Figure 5

Overview of the biological roles of N and known sparing and recycling mechanisms.

Figure 6

Overview of the biological roles of S and known sparing and recycling mechanisms.

Figure 7

Overview of the biological roles of P and known sparing and recycling mechanisms.

Figure 8

Overview of the biological roles of Fe and known sparing and recycling mechanisms.

Figure 9

Overview of the biological roles of Zn and known sparing and recycling mechanisms.

Figure 10

Overview of the biological role of Cu and known sparing and recycling mechanisms.

Figure 11

Overview of the biological roles of Co (B12) and Ni and known sparing mechanisms.

Figure 12

Overview of the biological roles of Mo (W) and Se and known sparing mechanisms.

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Elemental economy: microbial strategies for optimizing growth in the face of nutrient limitation - PubMed (original) (raw)