Big box, small box: bacteria either have all around big niches or all around small niches.

Soil prokaryotes are locked into two mutually exclusive types of niches: multidimensional generalization and specialization. In our recent paper, we discuss the implications for prokaryote evolution, community dominance, and network structure.
Published in Ecology & Evolution
Big box, small box: bacteria either have all around big niches or all around small niches.

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The world is made up of a bunch of different environmental conditions, like how much water is available, how acidic the soil is, how hot it is, etc. To live and reproduce, species need to successfully navigate all these different environmental conditions. How many kinds of environmental conditions species can exist in determines their “niche.” Species that can exist in a wide range of environmental conditions are “generalists” and those that only exist in a narrow range are “specialists.” Understanding whether species are generalists or specialists should consider their ability to exist across all these different environmental conditions (i.e., multidimensionality).  

We looked at the multidimensional niches of >1200 prokaryotes across the continental United States. This was made possible by the recent launch of the National Science Foundation's flagship repository of extensive environmental and ecological data, National Ecological Observatory Network (NEON). With NEON data, we assessed whether generalization and specialization are multidimensional processes in which species either only generalize (i.e., multidimensional generalization) or only specialize (i.e., multidimensional specialization) on all niche dimensions.  

You might be asking “Why should we care if multidimensional specialization and generalization is common?” Which is a fair question as it does seem abstract. Talking about dimensions brings up Sci-Fi-esque feelings and that's without bringing up the industry term for multidimensionality – hypervolume – that has always reminded me more of Star Trek than actual science. But the reason why this matters is that, if multidimensional specialization and generalization exist, then the environmental conditions that species can withstand increase and decrease exponentially. For example, if we just look at three different dimensions (e.g., water, temperature, and pH), multidimensional generalization increases the kinds of suitable habitat to the power of three (i.e., the number of dimensions)! Whereas multidimensional specialization decreases suitable habitat by the power of 1/3 (i.e., cubed). That has massive implications for what kinds of habitats species would find suitable with multidimensional generalists being resilient to environmental change and multidimensional specialists being very sensitive since any slight deviation in any one environmental condition would make a habitat unsuitable. So, we asked: 1) how common is multidimensional generalization and specialization and then 2) what are the implications of multidimensional specialization and generalization for prokaryotic evolution, community composition, and community structure. 

We found that ~90% of prokaryotes are in fact either multidimensional generalists or multidimensional specialists (Figure 1a). This indicates that multidimensional generalization and specialization are almost universal, opposing niche trajectories in soil prokaryotes where specialization (or generalization) on one dimension has consequences for other dimensions. Multidimensional specialization and generalization as opposing trajectories is further supported by how multidimensional specialization and generalization evolve (Figure 1b). We found that multidimensional specialization and generalization are highly conserved across prokaryotes with transitions from generalist to specialist (and vice versa) occurring 90% less often than random chance. This then raises an interesting question about why these two niche trajectories are conserved. We think that multidimensional generalist and specialist lifestyles are conserved because ecological strategies to specialize (or generalize) in one niche dimension may have consequences for specialization and generalization in all other important niche dimensions. Consequently, our finding that multidimensional generalization and specialization are ubiquitous, mutually exclusive, and conserved features of prokaryotic ecology opens new lines of research. For example, are ecological strategies for generalization and specialization incompatible so that, if selection forces a species to specialize on one dimension, a species has a harder time following generalist strategies in other dimensions (e.g., if a microbe has to make spores to specialize in drought conditions, that spore-forming strategy makes it harder to be a generalist in other dimensions like temperature). 

Figure 1. Multidimensional specialization and generalization are universal and evolutionarily conserved. A) Heatmap of niche breadth across four important dimensions of microbial ecology for >1200 soil prokaryotes. Niche breadth across all dimensions are highly correlated with groupings of taxa at the generalist and specialist extremes. Darker colors reflect higher niche breadth. B) Measure of phylogenetic conservation (LIPA Moran’s I) of average niche breadth with a smoothing line showing a quadratic relationship (i.e., the more specialized or generalized a taxon is, the stronger the phylogenetic signal for niche breadth). The quadratic relationship indicates that specialization and generalization are evolutionarily conserved because LIPA Moran’s I is higher at the specialized and generalized extremes as opposed to intermediate levels of niche breadth. The greater the LIPA Moran’s I, the more related taxa are the more similar their niche breadths (i.e., phylogenetic conservation of niche breadth). Each point represents one taxon. This plot is one example from 100 possible trees which all show the same relationship. The line is a LOESS fit that more closely resembles a quadratic than linear fit (two-tailed Wilcoxon signed-rank test, V = 0, P < 2.20 × 10–16). 

We then asked what these conserved, opposing niche trajectories mean for how species are organized in their communities. First, we found that multidimensional generalists dominate their communities by being 73-times more abundant than multidimensional specialists (Figure 2a). The dominance of multidimensional generalists is likely to increase resilience of microbiomes because the organisms that have the most flexible niche requirements – the multidimensional generalists – make up most of their communities. So, if there is a change to their environment, this means that communities predominantly consist of microbes that have leeway to deal with these environmental changes. However, when we looked at how these communities are structured, we found that multidimensional specialists are almost twice as structurally important on average than multidimensional generalists (Figure 2c). Specifically, these microbes associate with nearly double the number of other microbes in the network of community interactions, and these microbes are known to provide important community services, like detoxification and nutrient cycling, that structure community dynamics and ecosystem services (Figure 2d). This suggests that, while a lot of the community may be flexible in terms of environmental conditions (i.e., the multidimensional generalists), the microbes that define and structure these communities are more likely to be extra sensitive to environmental disturbances because their niches are constrained in multiple dimensions. So, most of the community may be very flexible, but the structurally important microbes may be especially sensitive. Does this mean that the many benefits microbiomes provide are sensitive or resilient to changing environmental conditions? Future work understanding what matters more for community stability will be important, such as asking: is community stability mostly impacted by the dominance of multidimensional generalists, the services provided by specialists, or does it depend on whether the specific ecosystem relies on generalist or specialist services?

Figure 2. Multidimensional specialization and generalization shape prokaryotic community composition and structure. A) Box plot of taxon abundance for multidimensional specialists (light purple) and generalists (dark purple). Multidimensional generalists are, on average, 73-times more abundant than multidimensional specialists (Z = -6.2806, p < 0.0001). Statistics are from permutational testing. X-axis is on a log10 scale. Box plots show the median (middle line) and the interquartile range (box). B) Schematic of network analysis. Larger circles represent taxa with higher degree centrality (i.e., number of connections with other microbes in network) and darker colors represent taxa with greater niche breadth. The hypothesis is that more specialized taxa (lighter colors) will have more connections (larger circles) than generalized taxa. C) Violin plot of degree centrality between multidimensional specialists and generalists. Multidimensional specialists are often more connected in their networks than generalists suggesting they play important structural roles in their communities. D) Bar graph of prokaryotic orders and the percent of those orders that are multidimensional specialists (number of “species” that are specialist in an order/number of “species” detected in that order). The null expectation is gray, the orders are purple. Icons next to the bars reflect the community services provided by the specialists in that order that were found in a literature review.Plant growth promotion” (leaf icon) includes bacteria that increase plant growth or improve plant defense. Detoxification” (skull icon) includes heavy metal immobilization, xenobiotic degradation and hydrocarbon degradation. Nutrient addition” (bacteria icon) includes important biogeochemical cycling processes such as carbon fixation, denitrification, sulfate reduction and nitrogen fixation. Complex carbon catabolism” (organic molecule icon) includes breakdown of complex, difficult to metabolize carbon sources such as lignin, chitin and cellulose. 

Putting it all together, generalization and specialization are not only common in soil prokaryotes, but they are also mutually exclusive processes, suggesting that specializing or generalizing on any one dimension means developing ecological strategies that make it hard to do the opposite on other dimensions. Further, these opposing niche trajectories also shape 1) how prokaryotes evolve with multidimensional specialization and generalization seemingly locking species into one of these two trajectories and 2) how communities are structured with microbiomes being dominated by multidimensional generalists while multidimensional specialists do the heavy lifting of structuring communities.  


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