Bottom-Up Effects on Biomass Versus Top-Down Effects on Identity: A Multiple-Lake Fish Community Manipulation Experiment

The extent to which ecosystems are regulated by top-down relative to bottom-up control has been a dominant paradigm in ecology for many decades. For lakes, it has been shown that predation by fish is an important determinant of variation in zooplankton and phytoplankton community characteristics. Effects of fish are expected to not only be a function of total fish biomass, but also of functional composition of the fish community. Previous research on the importance of trophic cascades in lakes has largely focused on the role of zooplanktivorous and piscivorous fish. We conducted a large-scale multiple-lake fish community manipulation experiment to test for the effect of differences in fish functional community composition on the trophic structure of lakes. We examine the effect of top-down and bottom-up factors on phytoplankton and zooplankton biomass as well as on their community composition. We put our data in a broader perspective by comparing our results to data of a survey that also included ponds with low fish densities as well as ponds with very high densities of fish. Our results indicate that the overall food web structure under relative high fish densities is primarily structured by bottom-up factors, whereas community characteristics seem to be primarily regulated by top-down factors. Our results suggest a subtle interplay between bottom-up and top-down factors, in which bottom-up factors dominate in determining quantities while top-down effects are important in determining identities of the communities.     

Comparative and experimental approaches to top-down and bottom-up regulation of bacteria

The regulation of bacterial community biomass and productivity by resources and predators is a central concern in the study of microbial food webs. Resource or bottom-up regulation refers to the limitation of bacteria by carbon and nutrients derived from allocthonous inputs, primary production, and heterotrophic production. Predatory or top-down regulation refers to the limitation of bacteria below levels supportable by resources alone. Large scale comparative studies demonstrate strong correlations between bacterial productivity and biomass, suggesting significant resource regulation. Comparisons of the abundances of heterotrophic flagellates and bacteria, however, imply that in some cases there may be top-down regulation of bacteria in eutrophic environments. Experimental studies in lakes support the importance of resource regulation and reveal little top-down control from protozoans. Increases in bacterial abundance and production with nutrient enrichment were limited in enclosure experiments with high abundances of the cladoceran, Daphnia. Regulation of bacteria by Daphnia may occur in many lakes seasonally and prevail in some lakes throughout the year where these animals sustain dense populations. In most situations, however, bacteria appear to be limited primarily by resources.     

Trophic interactions between viruses, bacteria and nanoflagellates under various nutrient conditions and simulated climate change

Population dynamics in the microbial food web are influenced by resource availability and predator/parasitism activities. Climatic changes, such as an increase in temperature and/or UV radiation, can also modify ecological systems in many ways. A series of enclosure experiments was conducted using natural microbial communities from a Mediterranean lagoon to assess the response of microbial communities to top-down control [grazing by heterotrophic nanoflagellates (HNF), viral lysis] and bottom-up control (nutrients) under various simulated climatic conditions (temperature and UV-B radiations). Different biological assemblages were obtained by separating bacteria and viruses from HNF by size fractionation which were then incubated in whirl-Pak bags exposed to an increase of 3°C and 20% UV-B above the control conditions for 96 h. The assemblages were also provided with an inorganic and organic nutrient supply. The data show (i) a clear nutrient limitation of bacterial growth under all simulated climatic conditions in the absence of HNF, (ii) a great impact of HNF grazing on bacteria irrespective of the nutrient conditions and the simulated climatic conditions, (iii) a significant decrease in burst size (BS) (number of intracellular lytic viruses per bacterium) and a significant increase of VBR (virus to bacterium ratio) in the presence of HNF, and (iv) a much larger temperature effect than UV-B radiation effect on the bacterial dynamics. These results show that top-down factors, essentially HNF grazing, control the dynamics of the lagoon bacterioplankton assemblage and that short-term simulated climate changes are only a secondary effect controlling microbial processes.     

Host-associated and free-living phage communities differ profoundly in phylogenetic composition

Phylogenetic profiling has been widely used for comparing bacterial communities, but has so far been impossible to apply to viruses because of the lack of a single marker gene analogous to 16S rRNA. Here we developed a reference tree approach for matching viral sequences and applied it to the largest viral datasets available. The resulting technique, Shotgun UniFrac, was used to compare host-associated and non-host-associated phage communities (130 total metagenomes), and revealed a profound split similar to that found with bacterial communities. This new informatics approach complements analysis of bacterial communities and promises to provide new insights into viral community dynamics, such as top-down versus bottom-up control of bacterial communities by viruses in a range of systems.     

Relationship between bacterial community composition and bottom-up versus top-down variables in four eutrophic shallow lakes

Bacterial community composition was monitored in four shallow eutrophic lakes during one year using denaturing gradient gel electrophoresis (DGGE) of PCR-amplified prokaryotic rDNA genes. Of the four lakes investigated, two were of the clearwater type and had dense stands of submerged macrophytes while two others were of the turbid type characterized by the occurrence of phytoplankton blooms. One turbid and one clearwater lake had high nutrient levels (total phosphorus, >100 micro g liter(-1)) while the other lakes had relatively low nutrient levels (total phosphorus, <100 micro g liter(-1)). For each lake, seasonal changes in the bacterial community were related to bottom-up (resources) and top-down (grazers) variables by using canonical correspondence analysis (CCA). Using an artificial model dataset to which potential sources of error associated with the use of relative band intensities in DGGE analysis were added, we found that preferential amplification of certain rDNA genes over others does not obscure the relationship between bacterial community composition and explanatory variables. Besides, using this artificial dataset as well as our own data, we found a better correlation between bacterial community composition and explanatory variables by using relative band intensities compared to using presence/absence data. While bacterial community composition was related to phytoplankton biomass in the high-nutrient lakes no such relation was found in the low-nutrient lakes, where the bacterial community is probably dependent on other organic matter sources. We used variation partitioning to evaluate top-down regulation of bacterial community composition after bottom-up regulation has been accounted for. Using this approach, we found no evidence for top-down regulation of bacterial community composition in the turbid lakes, while grazing by ciliates and daphnids (Daphnia and Ceriodaphnia) was significantly related to changes in the bacterial community in the clearwater lakes. Our results suggest that in eutrophic shallow lakes, seasonality of bacterial community structure is dependent on the dominant substrate source as well as on the food web structure.     

Rapid successions affect microbial N-acetyl-glucosamine uptake patterns during a lacustrine spring phytoplankton bloom

The vernal successions of phytoplankton, heterotrophic nanoflagellates (HNF) and viruses in temperate lakes result in alternating dominance of top-down and bottom-up factors on the bacterial community. This may lead to asynchronous blooms of bacteria with different life strategies and affect the channelling of particular components of the dissolved organic matter (DOM) through microbial food webs. We followed the dynamics of several bacterial populations and of other components of the microbial food web throughout the spring phytoplankton bloom period in a pre-alpine lake, and we assessed bacterial uptake patterns of two constituents of the labile DOM pool (N-acetyl-glucosamine [NAG] and leucine). There was a clear genotypic shift within the bacterial assemblage, from fast growing Cytophaga-Flavobacteria (CF) affiliated with Fluviicola and from Betaproteobacteria (BET) of the Limnohabitans cluster to more grazing resistant AcI Actinobacteria (ACT) and to filamentous morphotypes. This was paralleled by successive blooms of viruses and HNF. We also noted the transient rise of other CF (related to Cyclobacteriaceae and Sphingobacteriaceae) that are not detected by fluorescence in situ hybridization with the general CF probe. Both, the average uptake rates of leucine and the fractions of leucine incorporating bacteria were approximately five to sixfold higher than of NAG. However, the composition of the NAG-active community was much more prone to genotypic successions, in particular of bacteria with different life strategies: While 'opportunistically' growing BET and CF dominated NAG uptake in the initial period ruled by bottom-up factors, ACT constituted the major fraction of NAG active cells during the subsequent phase of high predation pressure. This indicates that some ACT could profit from a substrate that might in parts have originated from the grazing of protists on their bacterial competitors.     

Population Dynamics and Diversity of Viruses,Bacteria and Phytoplankton in a Shallow Eutrophic Lake

We have studied the temporal variation in viral abundances and community assemblage in the eutrophic Lake Loosdrecht through epifluorescence microscopy and pulsed field gel electrophoresis (PFGE). The virioplankton community was a dynamic component of the aquatic community, with abundances ranging between 5.5 x 10(7) and 1.3 x 10(8) virus-like particles ml(-1) and viral genome sizes ranging between 30 and 200 kb. Both viral abundances and community composition followed a distinct seasonal cycle, with high viral abundances observed during spring and summer. Due to the selective and parasitic nature of viral infection, it was expected that viral and host community dynamics would covary both in abundances and community composition. The temporal dynamics of the bacterial and cyanobacterial communities, as potential viral hosts, were studied in addition to a range of environmental parameters to relate these to viral community dynamics. Cyanobacterial and bacterial communities were studied applying epifluorescence microscopy, flow cytometry, and denaturing gradient gel electrophoresis (DGGE). Both bacterial and cyanobacterial communities followed a clear seasonal cycle. Contrary to expectations, viral abundances were neither correlated to abundances of the most dominant plankton groups in Lake Loosdrecht, the bacteria and the filamentous cyanobacteria, nor could we detect a correlation between the assemblage of viral and bacterial or cyanobacterial communities during the overall period. Only during short periods of strong fluctuations in microbial communities could we detect viral community assemblages to covary with cyanobacterial and bacterial communities. Methods with a higher specificity and resolution are probably needed to detect the more subtle virus-host interactions. Viral abundances did however relate to cyanobacterial community assemblage and showed a significant positive correlation to Chl-a as well as prochlorophytes, suggesting that a significant proportion of the viruses in Lake Loosdrecht may be phytoplankton and more specific cyanobacterial viruses. Temporal changes in bacterial abundances were significantly related to viral community assemblage, and vice versa, suggesting an interaction between viral and bacterial communities in Lake Loosdrecht.     

Variability in Microbial Community Composition and Function Between Different Niches Within a Coral Reef

To explore how microbial community composition and function varies within a coral reef ecosystem, we performed metagenomic sequencing of seawater from four niches across Heron Island Reef, within the Great Barrier Reef. Metagenomes were sequenced from seawater samples associated with (1) the surface of the coral species Acropora palifera, (2) the surface of the coral species Acropora aspera, (3) the sandy substrate within the reef lagoon and (4) open water, outside of the reef crest. Microbial composition and metabolic function differed substantially between the four niches. The taxonomic profile showed a clear shift from an oligotroph-dominated community (e.g. SAR11, Prochlorococcus, Synechococcus) in the open water and sandy substrate niches, to a community characterised by an increased frequency of copiotrophic bacteria (e.g. Vibrio, Pseudoalteromonas, Alteromonas) in the coral seawater niches. The metabolic potential of the four microbial assemblages also displayed significant differences, with the open water and sandy substrate niches dominated by genes associated with core house-keeping processes such as amino acid, carbohydrate and protein metabolism as well as DNA and RNA synthesis and metabolism. In contrast, the coral surface seawater metagenomes had an enhanced frequency of genes associated with dynamic processes including motility and chemotaxis, regulation and cell signalling. These findings demonstrate that the composition and function of microbial communities are highly variable between niches within coral reef ecosystems and that coral reefs host heterogeneous microbial communities that are likely shaped by habitat structure, presence of animal hosts and local biogeochemical conditions.     

Relationship between Bacterial Community Composition and Bottom-Up versus Top-Down Variables in Four Eutrophic Shallow Lakes

Bacterial community composition was monitored in four shallow eutrophic lakes during one year using denaturing gradient gel electrophoresis (DGGE) of PCR-amplified prokaryotic rDNA genes. Of the four lakes investigated, two were of the clearwater type and had dense stands of submerged macrophytes while two others were of the turbid type characterized by the occurrence of phytoplankton blooms. One turbid and one clearwater lake had high nutrient levels (total phosphorus, >100 μg liter⁻¹) while the other lakes had relatively low nutrient levels (total phosphorus, <100 μg liter⁻¹). For each lake, seasonal changes in the bacterial community were related to bottom-up (resources) and top-down (grazers) variables by using canonical correspondence analysis (CCA). Using an artificial model dataset to which potential sources of error associated with the use of relative band intensities in DGGE analysis were added, we found that preferential amplification of certain rDNA genes over others does not obscure the relationship between bacterial community composition and explanatory variables. Besides, using this artificial dataset as well as our own data, we found a better correlation between bacterial community composition and explanatory variables by using relative band intensities compared to using presence/absence data. While bacterial community composition was related to phytoplankton biomass in the high-nutrient lakes no such relation was found in the low-nutrient lakes, where the bacterial community is probably dependent on other organic matter sources. We used variation partitioning to evaluate top-down regulation of bacterial community composition after bottom-up regulation has been accounted for. Using this approach, we found no evidence for top-down regulation of bacterial community composition in the turbid lakes, while grazing by ciliates and daphnids (Daphnia and Ceriodaphnia) was significantly related to changes in the bacterial community in the clearwater lakes. Our results suggest that in eutrophic shallow lakes, seasonality of bacterial community structure is dependent on the dominant substrate source as well as on the food web structure.     

Deep sea sediments associated with cold seeps are a subsurface reservoir of viral diversity

In marine ecosystems, viruses exert control on the composition and metabolism of microbial communities, influencing overall biogeochemical cycling. Deep sea sediments associated with cold seeps are known to host taxonomically diverse microbial communities, but little is known about viruses infecting these microorganisms. Here, we probed metagenomes from seven geographically diverse cold seeps across global oceans to assess viral diversity, virus–host interaction, and virus-encoded auxiliary metabolic genes (AMGs). Gene-sharing network comparisons with viruses inhabiting other ecosystems reveal that cold seep sediments harbour considerable unexplored viral diversity. Most cold seep viruses display high degrees of endemism with seep fluid flux being one of the main drivers of viral community composition. In silico predictions linked 14.2% of the viruses to microbial host populations with many belonging to poorly understood candidate bacterial and archaeal phyla. Lysis was predicted to be a predominant viral lifestyle based on lineage-specific virus/host abundance ratios. Metabolic predictions of prokaryotic host genomes and viral AMGs suggest that viruses influence microbial hydrocarbon biodegradation at cold seeps, as well as other carbon, sulfur and nitrogen cycling via virus-induced mortality and/or metabolic augmentation. Overall, these findings reveal the global diversity and biogeography of cold seep viruses and indicate how viruses may manipulate seep microbial ecology and biogeochemistry.Subject terms: Environmental microbiology, Microbial ecology     

Surface Water Linkages Regulate Trophic Interactions in a Groundwater Food Web

Groundwaters are increasingly viewed as resource-limited ecosystems in which fluxes of dissolved organic carbon (DOC) from surface water are efficiently mineralized by a consortium of microorganisms which are grazed by invertebrates. We tested for the effect of groundwater recharge on resource supply and trophic interactions by measuring physico-chemistry, microbial activity and biomass, structure of bacterial communities and invertebrate density at three sites intensively recharged with surface water. Comparison of measurements made in recharge and control well clusters at each site showed that groundwater recharge significantly increased fluxes of DOC and phosphate, elevated groundwater temperature, and diminished dissolved oxygen (DO). Microbial biomass and activity were significantly higher in recharge well clusters but stimulation of autochthonous microorganisms was not associated with a major shift in bacterial community structure. Invertebrate assemblages were not significantly more abundant in recharge well clusters and did not show any relationship with microbial biomass and activity. Microbial communities were bottom-up regulated by DOC and nutrient fluxes but trophic interactions between microorganisms and invertebrates were apparently limited by environmental stresses, particularly DO depletion and groundwater warming. Hydrological connectivity is a key factor regulating the function of DOC-based groundwater food webs as it influences both resource availability for microorganisms and environmental stresses which affect energy transfer to invertebrates and top-down control on microorganisms.     

Symbiosis and the Regulation of Communities

Ecologists have long been interested in factors that controlthe structure of communities and the relative importance oftop-down effects of predators versus bottom-up effects of resources.There is a growing body of evidence that microbial symbiosesare important determinants of plant community structure andindirectly affect herbivore and predator trophic levels. Studieswith mycorrhizal fungi, N-fixing bacteria and endophytes ofgrasses have demonstrated that they can affect competition,coexistence, soil nutrient dynamics and plant-herbivore interactions.Long-term field experiments with one grass/endophyte interactionsuggest that grassland community structure is determined bythe fungus. While total plant productivity of experimental plotswas similar, the composition of the vegetation was altered byendophyte symbiosis. The host grass tall fescue (Festuca arundinacea)dominated plots when infected while other grasses greatly increasedin uninfected plots. Indirect evidence suggests that changesin prairie vole (Microtus ochrogaster) grazing patterns andreproductive physiology may be in part responsible for vegetationalchanges. These results provide evidence that, in addition tobottom-up and top-down forces, microbial symbionts of plantsare important determinants of community structure.     

On the different nature of top-down and bottom-up effects in pelagic food webs

SUMMARY 1. Each individual planktonic plant or animal is exposed to the hazards of starvation and risk of predation, and each planktonic population is under the control of resource limitation from the bottom up (growth and reproduction) and by predation from the top down (mortality). While the bottom-up and top-down impacts are traditionally conceived as compatible with each other, field population-density data on two coexisting Daphnia species suggest that the nature of the two impacts is different. Rates of change, such as the rate of individual body growth, rate of reproduction, and each species' population growth rate, are controlled from the bottom up. State variables, such as biomass, individual body size and population density, are controlled from the top down and are fixed at a specific level regardless of the rate at which they are produced.
2. According to the theory of functional responses, carnivorous and herbivorous predators react to prey density rather than to the rate at which prey are produced or reproduced. The predator's feeding rate (and thus the magnitude of its effect on prey density) should hence be regarded as a functional response to increasing resource concentration.
3. The disparity between the bottom-up and top-down effects is also apparent in individual decision making, where a choice must be made between accepting the hazards of hunger and the risks of predation (lost calories versus loss of life).
4. As long as top-down forces are effective, the disparity with bottom-up effects seems evident. In the absence of predation, however, all efforts of an individual become subordinate to the competition for resources. Biomass becomes limited from the bottom up as soon as the density of a superior competitor has increased to the carrying capacity of a given habitat. Such a shift in the importance of bottom-up control can be seen in zooplankton in habitats from which fish have been excluded.     

Gut microbial diversity across a contact zone for California voles: Implications for lineage divergence of hosts and mitonuclear mismatch in the assembly of the mammalian gut microbiome

Gut microbial diversity is thought to reflect the co‐evolution of microbes and their hosts as well as current host‐specific attributes such as genetic background and environmental setting. To explore interactions among these parameters, we characterized variation in gut microbiome composition of California voles (Microtus californicus) across a contact zone between two recently diverged lineages of this species. Because this contact zone contains individuals with mismatched mitochondrial‐nuclear genomes (cybrids), it provides an important opportunity to explore how different components of the genotype contribute to gut microbial diversity. Analyses of bacterial 16S rRNA sequences and joint species distribution modelling revealed that host genotypes and genetic differentiation among host populations together explained more than 50% of microbial community variation across our sampling transect. The ranked importance (most to least) of factors contributing to gut microbial diversity in our study populations were: genome‐wide population differentiation, local environmental conditions, and host genotypes. However, differences in microbial communities among vole populations (β‐diversity) did not follow patterns of lineage divergence (i.e., phylosymbiosis). Instead, among‐population variation was best explained by the spatial distribution of hosts, as expected if the environment is a primary source of gut microbial diversity (i.e., dispersal limitation hypothesis). Across the contact zone, several bacterial taxa differed in relative abundance between the two parental lineages as well as among individuals with mismatched mitochondrial and nuclear genomes. Thus, genetic divergence among host lineages and mitonuclear genomic mismatches may also contribute to microbial diversity by altering interactions between host genomes and gut microbiota (i.e., hologenome speciation hypothesis).     

Seasonal variation in top-down and bottom-up processes in a grassland arthropod community

Both top-down and bottom-up processes are common in terrestrial ecosystems, but how these opposing forces interact and vary over time is poorly understood. We tested the variation of these processes over seasonal time in a natural temperate zone grassland, a field site characterized by strong seasonal changes in abiotic and biotic conditions. Separate factorial experiments manipulating nutrients and cursorial spiders were performed in the wet and dry seasons. We also performed a water-addition experiment during the summer (dry season) to determine the degree of water limitation during this time. In the spring, nutrient addition increased plant growth and carnivore abundance, indicating a bottom-up control process. Among herbivores, sap-feeders were significantly enhanced while grazers significantly declined resulting in no net change in herbivore abundance. In the summer, water limitation was predominant increasing plants and all herbivores while nutrient (N) effects were non-significant. Top-down processes were present only in the spring season and only impacted the guild of grazing herbivores. These results show that bottom-up limitation is present throughout the season in this grassland, although the specific limiting resource changes as the season progresses. Bottom-up processes affected all trophic levels and many different guilds, while top-down effects were limited to a select group of herbivores and did not extend to the plant trophic level. Our results show that the relative strengths of top-down and bottom-up processes can shift over relatively short periods of time in habitats with a strong seasonal component.     

The dynamic genetic repertoire of microbial communities

Community genomic data have revealed multiple levels of variation between and within microbial consortia. This variation includes large-scale differences in gene content between ecosystems as well as within-population sequence heterogeneity. In the present review, we focus specifically on how fine-scale variation within microbial and viral populations is apparent from community genomic data. A major unresolved question is how much of the observed variation is due to neutral vs. adaptive processes. Limited experimental data hint that some of this fine-scale variation may be in part functionally relevant, whereas sequence-based and modeling analyses suggest that much of it may be neutral. While methods for interpreting population genomic data are still in their infancy, we discuss current interpretations of existing datasets in the light of evolutionary processes and models. Finally, we highlight the importance of virus–host dynamics in generating and shaping within-population diversity.     

Virioplankton: Viruses in Aquatic Ecosystems

The discovery that viruses may be the most abundant organisms in natural waters, surpassing the number of bacteria by an order of magnitude, has inspired a resurgence of interest in viruses in the aquatic environment. Surprisingly little was known of the interaction of viruses and their hosts in nature. In the decade since the reports of extraordinarily large virus populations were published, enumeration of viruses in aquatic environments has demonstrated that the virioplankton are dynamic components of the plankton, changing dramatically in number with geographical location and season. The evidence to date suggests that virioplankton communities are composed principally of bacteriophages and, to a lesser extent, eukaryotic algal viruses. The influence of viral infection and lysis on bacterial and phytoplankton host communities was measurable after new methods were developed and prior knowledge of bacteriophage biology was incorporated into concepts of parasite and host community interactions. The new methods have yielded data showing that viral infection can have a significant impact on bacteria and unicellular algae populations and supporting the hypothesis that viruses play a significant role in microbial food webs. Besides predation limiting bacteria and phytoplankton populations, the specific nature of virus-host interaction raises the intriguing possibility that viral infection influences the structure and diversity of aquatic microbial communities. Novel applications of molecular genetic techniques have provided good evidence that viral infection can significantly influence the composition and diversity of aquatic microbial communities.     

Experimental manipulations of microbial food web interactions in a humic lake: shifting biological drivers of bacterial community structure

A previous multiyear study observed correlations between bacterioplankton community composition (BCC) and abundance and the dynamics of phytoplankton populations and bacterivorous grazers in a humic lake. These observations generated hypotheses about the importance of trophic interactions (both top-down and bottom-up) for structuring bacterial communities in this lake, which were tested using two multifactorial food web manipulation experiments that separately manipulated the intensity of grazing and the composition of the phytoplankton community. Our results, combined with field observations, suggest that a hierarchy of drivers structures bacterial communities in this lake. While other studies have noted links between aggregate measures of phytoplankton and bacterioplankton communities, we demonstrate here correlations between succession of phytoplankton assemblages and BCC as assessed by automated ribosomal intergenic spacer analysis (ARISA). We used a novel approach linking community ARISA data to phylogenetic assignments from sequence analysis of 16S rRNA gene clone libraries to examine the responses of specific bacterial phylotypes to the experimental manipulations. The synchronous dynamics of these populations suggests that primary producers may mediate BCC and diversity through labile organic matter production, which evolves in quality and quantity during phytoplankton succession. Superimposed on this resource-mediated control of BCC are brief periods of intense bacterivory that impact bacterial abundance and composition.     

Viral biogeography revealed by signatures in Sulfolobus islandicus genomes

Viruses are a driving force of microbial evolution. Despite their importance, the evolutionary dynamics that shape diversity in viral populations are not well understood. One of the primary factors that define viral population structure is coevolution with microbial hosts. Experimental models predict that the trajectory of coevolution will be determined by the relative migration rates of viruses and their hosts; however, there are no natural microbial systems in which both have been examined. The biogeographic distribution of viruses that infect Sulfolobus islandicus is investigated using genome comparisons among four newly identified, integrated, Sulfolobus spindle-shaped viruses and previously sequenced viral strains. Core gene sequences show a biogeographic distribution where viral genomes are specifically associated with each local population. In addition, signatures of host–virus interactions recorded in the sequence-specific CRISPR (clustered regularly interspaced short palindromic repeats) system show that hosts have interacted with viral communities that are more closely related to local viral strains than to foreign ones. Together, both proviral and CRISPR sequences show a clear biogeographic structure for Sulfolobus viral populations. Our findings demonstrate that virus–microbe coevolution must be examined in a spatially explicit framework. The combination of host and virus biogeography suggests a model for viral diversification driven by host immunity and local adaptation.