Chemical defenses: from compounds to communities

Marine natural products play critical roles in the chemical defense of many marine organisms and in some cases can influence the community structure of entire ecosystems. Although many marine natural products have been studied for biomedical activity, yielding important information about their biochemical effects and mechanisms of action, much less is known about ecological functions. The way in which marine consumers perceive chemical defenses can influence their health and survival and determine whether some natural products persist through a food chain. This article focuses on selected marine natural products, including okadaic acid, brevetoxins, lyngbyatoxin A, caulerpenyne, bryostatins, and isocyano terpenes, and examines their biosynthesis (sometimes by symbiotic microorganisms), mechanisms of action, and biological and ecological activity. We selected these compounds because their impacts on marine organisms and communities are some of the best-studied among marine natural products. We discuss the effects of these compounds on consumer behavior and physiology, with an emphasis on neuroecology. In addition to mediating a variety of trophic interactions, these compounds may be responsible for community-scale ecological impacts of chemically defended organisms, such as shifts in benthic and pelagic community composition. Our examples include harmful algal blooms; the invasion of the Mediterranean by Caulerpa taxifolia; overgrowth of coral reefs by chemically rich macroalgae and cyanobacteria; and invertebrate chemical defenses, including the role of microbial symbionts in compound production.     

Bacterial Communities of Two Ubiquitous Great Barrier Reef Corals Reveals Both Site- and Species-Specificity of Common Bacterial Associates

Background

Coral-associated bacteria are increasingly considered to be important in coral health, and altered bacterial community structures have been linked to both coral disease and bleaching. Despite this, assessments of bacterial communities on corals rarely apply sufficient replication to adequately describe the natural variability. Replicated data such as these are crucial in determining potential roles of bacteria on coral.

Methodology/Principal Findings

Denaturing Gradient Gel Electrophoresis (DGGE) of the V3 region of the 16S ribosomal DNA was used in a highly replicated approach to analyse bacterial communities on both healthy and diseased corals. Although site-specific variations in the bacterial communities of healthy corals were present, host species-specific bacterial associates within a distinct cluster of gamma-proteobacteria could be identified, which are potentially linked to coral health. Corals affected by “White Syndrome” (WS) underwent pronounced changes in their bacterial communities in comparison to healthy colonies. However, the community structure and bacterial ribotypes identified in diseased corals did not support the previously suggested theory of a bacterial pathogen as the causative agent of the syndrome.

Conclusions/Significance

This is the first study to employ large numbers of replicated samples to assess the bacterial communities of healthy and diseased corals, and the first culture-independent assessment of bacterial communities on WS affected Acroporid corals on the GBR. Results indicate that a minimum of 6 replicate samples are required in order to draw inferences on species, spatial or health-related changes in community composition, as a set of clearly distinct bacterial community profiles exist in healthy corals. Coral bacterial communities may be both site and species specific. Furthermore, a cluster of gamma-proteobacterial ribotypes may represent a group of specific common coral and marine invertebrate associates. Finally, the results did not support the contention that a single bacterial pathogen may be the causative agent of WS Acroporids on the GBR.     

Diversity and dynamics of Antarctic marine microbial eukaryotes under manipulated environmental UV radiation

In the light of the predicted global climate change, it is essential that the status and diversity of polar microbial communities is described and understood. In the present study, molecular tools were used to investigate the marine eukaryotic communities of Prydz Bay, Eastern Antarctica, from November 2002 to January 2003. Additionally, we conducted four series of minicosm experiments, where natural Prydz Bay communities were incubated under six different irradiation regimes, in order to investigate the effects of natural UV radiation on marine microbial eukaryotes. Denaturing gradient gel electrophoresis (DGGE) and 18S rRNA gene sequencing revealed a eukaryotic Shannon diversity index averaging 2.26 and 2.12, respectively. Phylogenetic analysis of 472 sequenced clones revealed 47 phylotypes, belonging to the Dinophyceae, Stramenopiles, Choanoflagellidae, Ciliophora, Cercozoa and Metazoa. Throughout the studied period, three communities were distinguished: a postwinter/early spring community comprising dinoflagellates, ciliates, cercozoans, stramenopiles, viridiplantae, haptophytes and metazoans; a dinoflagellate-dominated community; and a diatom-dominated community that developed after sea ice breakup. DGGE analysis showed that size fraction and time had a strong shaping effect on the community composition; however, a significant contribution of natural UV irradiance towards microeukaryotic community composition could not be detected. Overall, dinoflagellates dominated our samples and their diversity suggests that they fulfill an important role in Antarctic coastal marine ecosystems preceding ice breakup as well as between phytoplankton bloom events.     

Evolution in metacommunities

A metacommunity can be defined as a set of communities that are linked by migration, and extinction and recolonization. In metacommunities, evolution can occur not only by processes that occur within communities such as drift and individual selection, but also by among-community processes, such as divergent selection owing to random differences among communities in species composition, and group and community-level selection. The effect of these among-community-level processes depends on the pattern of migration among communities. Migrating units may be individuals (migrant pool model), groups of individuals (single-species propagule pool model) or multi-species associations (multi-species propagule pool model). The most interesting case is the multi-species propagule pool model. Although this pattern of migration may a priori seem rare, it becomes more plausible in small well-defined 'communities' such as symbiotic associations between two or a few species. Theoretical models and experimental studies show that community selection is potentially an effective evolutionary force. Such evolution can occur either through genetic changes within species or through changes in the species composition of the communities. Although laboratory studies show that community selection can be important, little is known about how important it is in natural populations.     

Key role of selective viral-induced mortality in determining marine bacterial community composition

Viral infection is thought to play an important role in shaping bacterial community composition and diversity in aquatic ecosystems, but the strength of this interaction and the mechanisms underlying this regulation are still not well understood. The consensus is that viruses may impact the dominant bacterial strains, but there is little information as to how viruses may affect the less abundant taxa, which often comprise the bulk of the total bacterial diversity. The potential effect of viruses on the phylogenetic composition of marine bacterioplankton was assessed by incubating marine bacteria collected along a North Pacific coastal-open ocean transect in seawater that was greatly depleted of ambient viruses. The ambient communities were dominated by typical marine groups, including alphaproteobacteria and the Bacteroidetes. Incubation of these communities in virus-depleted ambient water yielded an unexpected and dramatic increase in the relative abundance of bacterial groups that are generally undetectable in the in situ assemblages, such as betaproteobacteria and Actinobacteria. Our results suggest that host susceptibility is not necessarily only proportional to its density but to other characteristics of the host, that rare marine bacterial groups may be more susceptible to viral-induced mortality, and that these rare groups may actually be the winners of competition for resources. These observations are not inconsistent with the 'phage kills the winner' hypothesis but represent an extreme and yet undocumented case of this paradigm, where the potential winners apparently never actually develop beyond a very low abundance threshold in situ. We further suggest that this mode of regulation may influence not just the distribution of single strains but of entire phylogenetic groups.     

The Physical Environment Affects Cyanophage Communities in British Columbia Inlets

Little is known about the natural distribution of viruses that infect the photosynthetically important group of marine prokaryotes, the cyanobacteria. The current investigation reveals that the structure of cyanophage communities is dependent on water column structure. PCR was used to amplify a fragment of the cyanomyovirus gene (g) 20, which codes for the portal vertex protein. Denaturing gradient gel electrophoresis (DGGE) of PCR amplified g20 gene fragments was used to examine variations in cyanophage community structure in three inlets in British Columbia, Canada. Qualitative examination of denaturing gradient gels revealed cyanophage community patterns that reflected the physical structure of the water column as indicated by temperature and salinity. Based on mobility of PCR fragments in the DGGE gels, some cyanophages appeared to be widespread, while others were observed only at specific depths. Cyanophage communities within Salmon Inlet were more related to one another than to communities from either Malaspina Inlet or Pendrell Sound. As well, surface communities in Malaspina Inlet and Pendrell Sound were different when compared to communities at depth. In the same two locations, distinct differences in community composition were observed in communities that coincided with depths of high chlorophyll fluorescence. The observed community shifts over small distances (only a few meters in depth or inlets separated by less than 100 km) support the idea that cyanophage communities separated by small spatial scales develop independently of each other as a result isolation by water column stratification or land mass separation, which may ultimately lead to changes in the distribution or composition of the host community. Present address (S.M. Short): Ocean Sciences Department, University of California, Santa Cruz 1156 High Street Santa Cruz, CA 95064; sshort@es.ucsc.edu     

Effects of pulse versus steady recruitment on sessile marine communities

Variation in patterns of propagule establishment (recruitment) has important effects on population dynamics and the structure of some communities. Most experimental studies have varied recruitment by changing the nature of a single event early in community development, but recruitment can also vary from steady rates of arrival to highly episodic 'pulse' events, causing differences in the temporal spacing of individuals recruiting into patches. We examined whether two different temporal patterns of recruitment of sessile invertebrates affected temperate marine communities in southeastern Australia in two experiments that were run at different times at the same site and that manipulated several different species. Target species entered communities as either a single pulse of recruits within a 2-week period or steady input of the same total number of recruits over a longer time period (5-6 weeks). The pattern of recruitment had variable effects on community structure. The colonial ascidian Botryllus schlosseri did not have a strong influence on community structure whether it recruited in a single pulse or steadily. The cover of B. schlosseri was higher when recruitment occurred as a single pulse. In a second experiment, botryllid ascidians caused changes in the composition of communities when they recruited steadily compared to when they did not recruit or didemnids recruited, but caused no differences in communities when they recruited in a shorter pulse. In contrast, recruitment frequency of didemnid ascidians had little effect, though their presence/absence caused community differences. Though we found that different temporal recruitment patterns can alter community composition, the life history and ecology of particular taxa as well as differences in environmental background processes are likely to influence the strength of these effects.     

Laboratory conditions can change the complexity and composition of the natural aquatic mycobiome on Alnus glutinosa leaf litter

Community structure is of major interest when aquatic fungi are studied, particularly in leaf decomposition experiments. Although such studies are often conducted as laboratory experiments with microbial communities taken from the field, it remains unclear to what extent natural fungal communities can be sustained under experimental conditions. Here, we used DNA metabarcoding to investigate the development of fungal communities on alder leaves both under laboratory and field conditions. Five leaf conditioning treatments were compared by colonizing leaves in a stream, exposing stream colonized leaves to a defined medium or filtered stream water and using stream colonized leaves to inoculate sterile leaves in the defined medium or stream water. Fewer species were found on leaves that were inoculated under laboratory conditions, whereas differences in fungal community composition were comparably low in the other treatments, irrespective of the chosen medium. Possible shifts in fungal communities should therefore be considered in laboratory experiments.     

Identification of a diagnostic marker to detect freshwater cyanophages of filamentous cyanobacteria

Cyanophages are viruses that infect the cyanobacteria, globally important photosynthetic microorganisms. Cyanophages are considered significant components of microbial communities, playing major roles in influencing host community diversity and primary productivity, terminating cyanobacterial water blooms, and influencing biogeochemical cycles. Cyanophages are ubiquitous in both marine and freshwater systems; however, the majority of molecular research has been biased toward the study of marine cyanophages. In this study, a diagnostic probe was developed to detect freshwater cyanophages in natural waters. Oligonucleotide PCR-based primers were designed to specifically amplify the major capsid protein gene from previously characterized freshwater cyanomyoviruses that are infectious to the filamentous, nitrogen-fixing cyanobacterial genera Anabaena and Nostoc. The primers were also successful in yielding PCR products from mixed virus communities concentrated from water samples collected from freshwater lakes in the United Kingdom. The probes are thought to provide a useful tool for the investigation of cyanophage diversity in freshwater environments.     

Marine bacterial,archaeal and protistan association networks reveal ecological linkages

Microbes have central roles in ocean food webs and global biogeochemical processes, yet specific ecological relationships among these taxa are largely unknown. This is in part due to the dilute, microscopic nature of the planktonic microbial community, which prevents direct observation of their interactions. Here, we use a holistic (that is, microbial system-wide) approach to investigate time-dependent variations among taxa from all three domains of life in a marine microbial community. We investigated the community composition of bacteria, archaea and protists through cultivation-independent methods, along with total bacterial and viral abundance, and physico-chemical observations. Samples and observations were collected monthly over 3 years at a well-described ocean time-series site of southern California. To find associations among these organisms, we calculated time-dependent rank correlations (that is, local similarity correlations) among relative abundances of bacteria, archaea, protists, total abundance of bacteria and viruses and physico-chemical parameters. We used a network generated from these statistical correlations to visualize and identify time-dependent associations among ecologically important taxa, for example, the SAR11 cluster, stramenopiles, alveolates, cyanobacteria and ammonia-oxidizing archaea. Negative correlations, perhaps suggesting competition or predation, were also common. The analysis revealed a progression of microbial communities through time, and also a group of unknown eukaryotes that were highly correlated with dinoflagellates, indicating possible symbioses or parasitism. Possible ‘keystone'' species were evident. The network has statistical features similar to previously described ecological networks, and in network parlance has non-random, small world properties (that is, highly interconnected nodes). This approach provides new insights into the natural history of microbes.     

Functional group diversity, resource preemption and the genesis of invasion resistance in a community of marine algae

Although many studies have investigated how community characteristics such as diversity and disturbance relate to invasibility, the mechanisms underlying biotic resistance to introduced species are not well understood. I manipulated the functional group composition of native algal communities and invaded them with the introduced, Japanese seaweed Sargassum muticum to understand how individual functional groups contributed to overall invasion resistance. The results suggested that space preemption by crustose and turfy algae inhibited S. muticum recruitment and that light preemption by canopy and understory algae reduced S. muticum survivorship. However, other mechanisms I did not investigate could have contributed to these two results. In this marine community the sequential preemption of key resources by different functional groups in different stages of the invasion generated resistance to invasion by S. muticum . Rather than acting collectively on a single resource the functional groups in this system were important for preempting either space or light, but not both resources. My experiment has important implications for diversity–invasibility studies, which typically look for an effect of diversity on individual resources. Overall invasion resistance will be due to the additive effects of individual functional groups (or species) summed over an invader's life cycle. Therefore, the cumulative effect of multiple functional groups (or species) acting on multiple resources is an alternative mechanism that could generate negative relationships between diversity and invasibility in a variety of biological systems.     

Identification of a Diagnostic Marker To Detect Freshwater Cyanophages of Filamentous Cyanobacteria

Cyanophages are viruses that infect the cyanobacteria, globally important photosynthetic microorganisms. Cyanophages are considered significant components of microbial communities, playing major roles in influencing host community diversity and primary productivity, terminating cyanobacterial water blooms, and influencing biogeochemical cycles. Cyanophages are ubiquitous in both marine and freshwater systems; however, the majority of molecular research has been biased toward the study of marine cyanophages. In this study, a diagnostic probe was developed to detect freshwater cyanophages in natural waters. Oligonucleotide PCR-based primers were designed to specifically amplify the major capsid protein gene from previously characterized freshwater cyanomyoviruses that are infectious to the filamentous, nitrogen-fixing cyanobacterial genera Anabaena and Nostoc. The primers were also successful in yielding PCR products from mixed virus communities concentrated from water samples collected from freshwater lakes in the United Kingdom. The probes are thought to provide a useful tool for the investigation of cyanophage diversity in freshwater environments.     

Context‐specific effects of the identity of detrital mixtures on invertebrate communities

Many aquatic ecosystems are sustained by detrital subsidies of leaf litter derived from exogenous sources. Although numerous studies have examined the effects of litter species richness and identity on decomposition processes, it remains unclear how these effects extend to associated invertebrate communities or how these effects vary spatially according to local environmental context. Using field enrichment experiments, we assessed how the species richness, assemblage composition, and supply of detrital litter resources interact to affect benthic communities of three temperate Australian estuarine mudflats. Our experiments utilized eight litter sources that are presently experiencing human‐mediated changes in their supply to estuarine mudflats. Contrary to predictions, we did not detect effects of the species richness of detrital mixtures on benthic communities. Macroinvertebrate community structure and, in particular, abundance were, instead, influenced by the assemblage composition of detrital mixtures. At two of the three sites, plots receiving the most labile detrital mix, containing the ephemeral algae Chaetomorpha and Ulva, supported the fewest macroinvertebrates of all the experimental enrichments. The large effect of detrital mix identity on macroinvertebrate communities is of concern given present trends of proliferation of macroalgae at the expense of more refractory seagrasses and marsh grasses. As such environmental degradation continues, it will be important to more fully understand under what environmental contexts such compositional changes in detrital resources will have the most detrimental effects on important prey resources for commercially important fish and wading shorebirds.     

Meta‐analysis on pulse disturbances reveals differences in functional and compositional recovery across ecosystems

Most ecosystems are affected by anthropogenic or natural pulse disturbances, which alter the community composition and functioning for a limited period of time. Whether and how quickly communities recover from such pulses is central to our understanding of biodiversity dynamics and ecosystem organisation, but also to nature conservation and management. Here, we present a meta‐analysis of 508 (semi‐)natural field experiments globally distributed across marine, terrestrial and freshwater ecosystems. We found recovery to be significant yet incomplete. At the end of the experiments, disturbed treatments resembled controls again when considering abundance (94%), biomass (82%), and univariate diversity measures (88%). Most disturbed treatments did not further depart from control after the pulse, indicating that few studies showed novel trajectories induced by the pulse. Only multivariate community composition on average showed little recovery: disturbed species composition remained dissimilar to the control throughout most experiments. Still, when experiments revealed a higher compositional stability, they tended to also show higher functional stability. Recovery was more complete when systems had high resistance, whereas resilience and resistance were negatively correlated. The overall results were highly consistent across studies, but significant differences between ecosystems and organism groups appeared. Future research on disturbances should aim to understand these differences, but also fill obvious gaps in the empirical assessments for regions (especially the tropics), ecosystems and organisms. In summary, we provide general evidence that (semi‐)natural communities can recover from pulse disturbances, but compositional aspects are more vulnerable to long‐lasting effects of pulse disturbance than the emergent functions associated to them.     

Use of Ultrafiltration To Isolate Viruses from Seawater Which Are Pathogens of Marine Phytoplankton

Viruses may be major structuring elements of phytoplankton communities and hence important regulators of nutrient and energy fluxes in aquatic environments. In order to ascertain whether viruses are potentially important in dictating phytoplankton community structure, it is essential to determine the extent to which representative phytoplankton taxa are susceptible to viral infection. We used a spiral ultrafiltration cartridge (30,000-molecular-weight cutoff) to concentrate viruses from seawater at efficiencies approaching 100%. Natural virus communities were concentrated from stations in the Gulf of Mexico, a barrier island pass, and a hypersaline lagoon (Laguna Madre) and added to cultures of potential phytoplankton hosts. By following changes in in vivo fluorescence over time, it was possible to isolate several viruses that were pathogens to a variety of marine phytoplankton, including a prasinophyte (Micromonas pusilla), a pennate diatom (likely a Navicula sp.), a centric diatom (of unknown taxa), and a chroococcoid cyanobacterium (a Synechococcus sp.). As well, we observed changes in fluorescence in cultures of a cryptophyte (a Rhodomonas sp.) and a chlorophyte (Nannochloropsis oculata) which were consistent with the presence of viral pathogens. Although pathogens were isolated from all stations, all the pathogens were not isolated from every station. Filterability studies on the viruses infecting M. pusilla and the Navicula sp. showed that the viruses were consistently infective after filtration through polycarbonate and glass-fiber filters but were affected by most other filter types. Establishment of phytoplankton-pathogen systems will be important in elucidating the effect that viruses have on primary producers in aquatic systems.     

Impact of UV radiation on bacterioplankton community composition

The potential effect of UV radiation on the composition of coastal marine bacterioplankton communities was investigated. Dilution cultures with seawater collected from the surface mixed layer of the coastal North Sea were exposed to different ranges of natural or artificial solar radiation for up to two diurnal cycles. The composition of the bacterioplankton community prior to exposure was compared to that after exposure to the different radiation regimes using denaturing gradient gel electrophoresis (DGGE) of 16S rRNA and 16S ribosomal DNA. Only minor changes in the composition of the bacterial community in the different radiation regimes were detectable. Sequencing of selected bands obtained by DGGE revealed that some species of the Flexibacter-Cytophaga-Bacteroides (FCB) group were sensitive to UV radiation while other species of the FCB group were resistant. Overall, only up to approximately 10% of the operational taxonomic units present in the dilution cultures appeared to be affected by UV radiation. Thus, we conclude that UV radiation has little effect on the composition of coastal marine bacterioplankton communities in the North Sea.     

Limited versus unlimited membership in microbial communities: evaluation and experimental tests of some paradigms

Recent developments in community ecology have allowed for the synthesis of community models based on principles of limited and unlimited membership. In this discussion, these developments are used as a framework for evaluating the validity of three paradigms that have constrained research on aquatic microbial communities. Because microbes are considered to possess global distributions, species availability is not generally considered to be an important factor determining microbial community composition in most habitats. Requirements for the global distribution of a species are not the same as those for unlimited availability. Rates of propagule transport to isolated and newly formed aquatic systems ( 4 years old) are low enough to have a strong effect on microbial community composition. Natural aquatic systems may require several years to accumulate a full complement of species adapted to environmental conditions at a particular time. Except under extreme circumstances, environmental conditions are not considered to constrain membership in aquatic microbial communities. Most evidence for this contention is based on an inability to detect simple relationships between species distributions and levels of individual environmental parameters. Environmental measurements are often made at a spatial scale much greater than that of the local environment of microbes. Biotic interactions, such as competition, are generally considered to be the predominant force structuring aquatic microbial communities. Although there is an extensive laboratory database to suggest the importance of different types of species interactions, there have been few field studies to confirm this. A general research protocol is described to test predictions derived from current theory of microbial community organization. A mesocosm approach is advocated in order to incorporate crucial aspects of environmental realism into experimental designs while maintaining some of the control found in the laboratory.     

Dinoflagellates,diatoms, and their viruses

Since the first discovery of the very high virus abundance in marine environments, a number of researchers were fascinated with the world of "marine viruses", which had previously been mostly overlooked in studies on marine ecosystems. In the present paper, the possible role of viruses infecting marine eukaryotic microalgae is enlightened, especially summarizing the most up-to-the-minute information of marine viruses infecting bloom-forming dinoflagellates and diatoms. To author's knowledge, approximately 40 viruses infecting marine eukaryotic algae have been isolated and characterized to different extents. Among them, a double-stranded DNA (dsDNA) virus "HcV" and a single-stranded RNA (ssRNA) virus "HcRNAV" are the only dinoflagellate-infecting (lytic) viruses that were made into culture; their hosts are a bivalve-killing dinoflagellate Heterocapsa circularisquama. In this article, ecological relationship between H. circularisquama and its viruses is focused. On the other hand, several diatom-infecting viruses were recently isolated and partially characterized; among them, one is infectious to a pen-shaped bloom-forming diatom species Rhizosolenia setigera; some viruses are infectious to genus Chaetoceros which is one of the most abundant and diverse diatom group. Although the ecological relationships between diatoms and their viruses have not been sufficiently elucidated, viral infection is considered to be one of the significant factors affecting dynamics of diatoms in nature. Besides, both the dinoflagellate-infecting viruses and diatom-infecting viruses are so unique from the viewpoint of virus taxonomy; they are remarkably different from any other viruses ever reported. Studies on these viruses lead to an idea that ocean may be a treasury of novel viruses equipped with fascinating functions and ecological roles.     

Phylogenetic diversity of marine cyanophage isolates and natural virus communities as revealed by sequences of viral capsid assembly protein gene g20

In order to characterize the genetic diversity and phylogenetic affiliations of marine cyanophage isolates and natural cyanophage assemblages, oligonucleotide primers CPS1 and CPS8 were designed to specifically amplify ca. 592-bp fragments of the gene for viral capsid assembly protein g20. Phylogenetic analysis of isolated cyanophages revealed that the marine cyanophages were highly diverse yet more closely related to each other than to enteric coliphage T4. Genetically related marine cyanophage isolates were widely distributed without significant geographic segregation (i.e., no correlation between genetic variation and geographic distance). Cloning and sequencing analysis of six natural virus concentrates from estuarine and oligotrophic offshore environments revealed nine phylogenetic groups in a total of 114 different g20 homologs, with up to six clusters and 29 genotypes encountered in a single sample. The composition and structure of natural cyanophage communities in the estuary and open-ocean samples were different from each other, with unique phylogenetic clusters found for each environment. Changes in clonal diversity were also observed from the surface waters to the deep chlorophyll maximum layer in the open ocean. Only three clusters contained known cyanophage isolates, while the identities of the other six clusters remain unknown. Whether or not these unidentified groups are composed of bacteriophages that infect different Synechococcus groups or other closely related cyanobacteria remains to be determined. The high genetic diversity of marine cyanophage assemblages revealed by the g20 sequences suggests that marine viruses can potentially play important roles in regulating microbial genetic diversity.     

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