Pathogen Specialization and Coevolution: Trade-Offs in Host Range from Fungal Biotrophs to Microbial Models

As noted at the outset, pathogenic microorganisms can be highly specialized as parasites of a single host species or, conversely, may have evolved as relative generalists to derive nutrition from hosts in many species or even families (Woolhouse et al. 2001; Barrett et al. 2009) (Fig. 3.9). To use fungi as an example, fungal phylogenies reveal that plant parasitic species frequently are closely related to species that live exclusively as saprobes or mutualists (Berbee 2001; James et al. 2006). Apart from having usually very narrow plant host ranges, the pathogens that are extreme specialists share several correlates. Among these are (i) a typically intimate association with their hosts that tends to result in minimal damage to the plant cells (indeed, some fungal parasites—the obligate biotrophs—are so nutritionally dependent on living host tissues that they cannot be cultivated on artificial media); (ii) close synchrony between host and parasite life cycle stages; and ultimately (iii) a tight coevolutionary relationship marked at the population level by coordination in genes for host resistance and parasite virulence (see the gene-for-gene relationship in earlier Sidebar). The endless spiral of specialization is most dramatically seen in agroecosystems, where the repeated introduction of resistant cultivars has been matched by corresponding evolution of new strains of the pathogen. Probably the most sophisticated specialists are those parasites that must alternate between two taxonomically distinct hosts to complete their life cycle. This is because they have to synchronize their developmental stages not only with one host but two quite different hosts (recall the rusts noted earlier and see Chap. 6).

Does the intense specialization evident in many coevolutionary relationships such as between herbivorous insects or plant parasites and their hosts reflect optimization in the sense of a precise fit between organism and its physical and biotic environment (as many adaptationists might argue)? Or are such examples an evolutionary dead-end, an endpoint in an ongoing spiral where the partners “each drive the other into an ever-deepening rut of specialization” (Harper 1982; see also Moran 1988, 1989)? Broadly speaking, phylogenies show that specialists are not always on the terminal branches, i.e., they are not necessarily a derived condition and such relationships may open successful new evolutionary avenues (Thompson 1994). This interesting issue will be explored in Chap. 6 where we take up the evolution of complex life cycles.

Summary.All creatures must acquire nutrient resources from their environment and then allocate them among the competing demands of growth, maintenance, and reproduction. Additionally, they must extract and transform energy needed in anabolism and catabolism, as well as maintenance of molecular complexity and orderliness. In doing so, they operate according to a very similar biochemical master plan and obey the same fundamental laws of thermodynamics, energy balance, and mass. Metabolic and stoichiometric rules are universal and metabolic rates largely determine the rates of most biological activities. However, the ways in which organisms obtain resources are multiple and a defining characteristic, so much so that mode of nutrition is one of the key criteria for the categorization of species at the kingdom level.

Resource categories can be illustrated by defined with respect to sources of energy and of carbon building blocks for an organism. ATP is the major carrier of biologically usable energy in all organisms and there are only two basic mechanisms for its generation: electron transport phosphorylation, or substrate-level phosphorylation. In phototrophs (phototrophic bacteria, algae, plants), energy is obtained directly from the sun, in which case light energy is converted by electron transport phosphorylation into the high-energy phosphate bonds of ATP. In chemotrophs (most organisms), ATP is generated from reduced inorganic compounds or from organic compounds by electron transport phosphorylation or substrate-level phosphorylation. Carbon is acquired either directly from CO₂ (autotrophs) or from organic compounds (heterotrophs). Although the resulting energy/carbon permutations form several potential resource categories, most living forms, in terms of species or biomass, use either light energy to fix CO₂ for their biosynthetic needs (photoautotrophs, e.g., plants), or derive both their energy (i.e., in this case electron donors) and carbon from organic molecules (chemoheterotrophs, e.g., animals and most microbes). Chemolithotrophs (chemotro- phs using an inorganic electron donor), which evidently exist only as microorganisms, and though apparently fewer in number of species, play an essential global role in biogeochemical cycles.

A manifestation of energy/nutrient relationships within the living world is the trophic structure of ecosystems. This is usually depicted as a grazer food chain or network based on phototrophs associated with a decomposer chain based on dead organic matter. Microbes play a key role in both, particularly the latter. Apart from the microscopic plankton in aquatic systems, however, their role in grazer systems has been underestimated until recently. The central role of an explicit ‘heterotrophic microbial loop,’ which converts dissolved organic matter to biomass that reenters the grazer chain, is now generally recognized in aquatic systems, as is a significant class of mixotrophic plankton that combine the functions of photoautotrophy and chemoheterotrophy. Likewise, historic depictions have not generally accommodated food chains based on other sources of energy input, most notably that fixed chemosynthetically by lithoautotrophic bacteria. These microbes can, for example, support substantial oases of benthic invertebrates around deep-sea hydrothermal vents, representing a novel, second major source for primary production on Earth.

The sources of energy and carbon also set broad limits on the distribution of living things, as in the restriction of aquatic plants, algae, and photosynthetic microbes to the euphotic zone, of obligate parasites to their hosts, and of many lithotrophic bacteria to their requisite geochemicals.

As originally devised, optimal foraging theory was essentially a cost/benefit analysis in energetic terms developed primarily as an economic optimization model to interpret the foraging behavior of certain animals. It can be construed broadly, merged with optimal digestion theory, and applied informally, conceptually, and empirically to all organisms. Formal, rigorous tests of the theory can and have been undertaken successfully but are relatively few. Broadly speaking, in terms of foraging, bacteria appear to do largely by metabolic versatility what animals accomplish by mobility and behavior, and plants, fungi, and other sessile organisms by morphology. Architecture and behavior are, however, compromise responses to many selection pressures, of which energy acquisition and allocation is only one. In the past two decades classic OFT has given way to increased focus on the search process per se, the extremes of which are random (as represented by Brownian walks or Levy walks) or systematic exploration. Both types of searches occur among microorganisms as well as macroorganisms.

From the standpoint of the individual and with respect to nutrition, versatility can be defined either as the ability to do many things, or to respond rapidly to new conditions. As judged by the first definition it cannot be said definitively whether microbes are more or less versatile than macro organisms because all of the metabolites for even a single life form are as yet unknown. Metabolic reconstructions are being projected based mainly on genomic annotations and exist for several prokaryotes and yeasts, and a few multicellular eukaryotes. Although the metabolic pathways and metabolites in some cell types of a multicellular eukaryotic organism may be comparatively few, in aggregate for the individual they likely exceed those for a microorganism, given the range of cell types, the subcellular compartmentaliza- tion, and the diversity of complex chemicals produced. When versatility is construed as speed of response, bacteria (and possibly some other microbes such as the fungi) appear to be more versatile metabolically than macro organisms because they can rapidly switch entire metabolic pathways.

Organisms are either relative generalists or specialists with respect to dietary range. For the generalist macroorganism with diverse prey items or the generalist microbe able to use many substrates, ‘food’ is potentially easier to find, substitutable resources can be alternated, search times are potentially shorter, and starvation is less likely. When food sources exert evolutionary pressure by their structural, behavioral, or physiological complexity, a specialized response by the consumer, such as restriction in dietary breadth, is a common result. This may be seen, for example, among individual bumblebees specializing as foragers on a particular flower type, by the coevolution of parasites with their hosts, and by specialist microbial strains that will not grow in the absence of a specific energy source. Broadly speaking, specializations offer advantages (optimization at doing certain things) but also impose disadvantages (fewer options). Evolution tends to move organisms towards increasing specialization, thereby narrowing options and limiting what they can do. Some of the best examples of specialization are found in coevolutionary relationships, where iterations involving the change in one partner (such as evolution of host resistance to parasites) are matched by corresponding changes in the other (evolution of virulence factors).

A corollary to optimal foraging theory is that generalists are predicted to be less efficient in finding and/or exploiting any particular resource than specialists on that resource. This has generally been accepted intuitively as reflected in the adage ‘the jack-of-all-trades is master of none’ and it has been documented with theoretical models going back to the early work of Robert MacArthur, among others. Nevertheless, trade-offs are not necessarily inherent and in some cases traits promoting performance in one environment do so also in others. The supporting evidence from field studies for trade-offs is mixed and subject to caveats. For example, there is difficulty in isolating the variable of interest (feeding range) with experimental systems of macroorganisms and, for microorganisms, in designing critical experiments (such as in determining how long it will take for trade-offs to manifest themselves), and in extrapolating the results of competition experiments between microbial strains judged to be generalists versus specialists under laboratory conditions to nature. A broader limitation is that organisms perform multiple tasks simultaneously and overall fitness is some aggregate function of which foraging is only one component.

Suggested Additional Reading: Alberts, B. et al. 2015. Molecular Biology of the Cell, 6th Ed. Garland Science, N.Y. Excellent overview of cellular biochemistry, structure, and genetics, including comparisons of prokaryotes and eukaryotes.

Caron, D.A. et al. 2017. Probing the evolution, ecology and physiology of marine protists using transcriptomics. Nature Rev. Microbiol. 15: 6-20. An excellent synthesis of marine protists and their role in the ecology of the oceans, including mixotrophy.

Gross, T. and H. Sayana (Eds.). 2009. Adaptive Networks: Theory, Models and Applications. Springer, NY. Attributes and commonalities among abiotic and biotic networks and branching systems.

Monk, J., J. Nogales, and B.O. Palsson. 2014. Optimizing genome-scale network reconstructions. Nature

Biotechnol. 32: 447-452. A comprehensive status report on knowledge of the projected metabolism for 78 species across the tree of life based largely on genome annotation.

Oceanography, vol. 20 no.2, June 2007. Special Issue: A Sea of Microbes. A good compendium of papers on the centrality of microorganisms in marine ecology. See also the compiled papers in “Microbial Carbon Pump in the Ocean" (eds. N. Jiao, F. Azam, S. Sanders) Supplement to Science, 13 May 2011; and M.A. Moran (2015), The global ocean microbiome. Science 350, doi:10.1126/science.aac8455