Viral predation pressure on coral reefs.

BACKGROUND: Predation pressure and herbivory exert cascading effects on coral reef health and stability. However, the extent of these cascading effects can vary considerably across space and time. This variability is likely a result of the complex interactions between coral reefs' biotic and abiotic dimensions. A major biological component that has been poorly integrated into the reefs' trophic studies is the microbial community, despite its role in coral death and bleaching susceptibility. Viruses that infect bacteria can control microbial densities and may positively affect coral health by controlling microbialization. We hypothesize that viral predation of bacteria has analogous effects to the top-down pressure of macroorganisms on the trophic structure and reef health. RESULTS: Here, we investigated the relationships between live coral cover and viruses, bacteria, benthic algae, fish biomass, and water chemistry in 110 reefs spanning inhabited and uninhabited islands and atolls across the Pacific Ocean. Statistical learning showed that the abundance of turf algae, viruses, and bacteria, in that order, were the variables best predicting the variance in coral cover. While fish biomass was not a strong predictor of coral cover, the relationship between fish and corals became apparent when analyzed in the context of viral predation: high coral cover (> 50%) occurred on reefs with a combination of high predator fish biomass (sum of sharks and piscivores > 200 g m-2) and high virus-to-bacteria ratios (> 10), an indicator of viral predation pressure. However, these relationships were non-linear, with reefs at the higher and lower ends of the coral cover continuum displaying a narrow combination of abiotic and biotic variables, while reefs at intermediate coral cover showed a wider range of parameter combinations. CONCLUSIONS: The results presented here support the hypothesis that viral predation of bacteria is associated with high coral cover and, thus, coral health and stability. We propose that combined predation pressures from fishes and viruses control energy fluxes, inhibiting the detrimental accumulation of ecosystem energy in the microbial food web.

A multiomic analysis of in situ coral-turf algal interactions.

Viruses, microbes, and host macroorganisms form ecological units called holobionts. Here, a combination of metagenomic sequencing, metabolomic profiling, and epifluorescence microscopy was used to investigate how the different components of the holobiont including bacteria, viruses, and their associated metabolites mediate ecological interactions between corals and turf algae. The data demonstrate that there was a microbial assemblage unique to the coral-turf algae interface displaying higher microbial abundances and larger microbial cells. This was consistent with previous studies showing that turf algae exudates feed interface and coral-associated microbial communities, often at the detriment of the coral. Further supporting this hypothesis, when the metabolites were assigned a nominal oxidation state of carbon (NOSC), we found that the turf algal metabolites were significantly more reduced (i.e., have higher potential energy) compared to the corals and interfaces. The algae feeding hypothesis was further supported when the ecological outcomes of interactions (e.g., whether coral was winning or losing) were considered. For example, coral holobionts losing the competition with turf algae had higher Bacteroidetes-to-Firmicutes ratios and an elevated abundance of genes involved in bacterial growth and division. These changes were similar to trends observed in the obese human gut microbiome, where overfeeding of the microbiome creates a dysbiosis detrimental to the long-term health of the metazoan host. Together these results show that there are specific biogeochemical changes at coral-turf algal interfaces that predict the competitive outcomes between holobionts and are consistent with algal exudates feeding coral-associated microbes.

The landscape of lysogeny across microbial community density, diversity and energetics.

Lysogens are common at high bacterial densities, an observation that contrasts with the prevailing view of lysogeny as a low-density refugium strategy. Here, we review the mechanisms regulating lysogeny in complex communities and show that the additive effects of coinfections, diversity and host energic status yield a bimodal distribution of lysogeny as a function of microbial densities. At high cell densities (above 106 cells ml-1 or g-1 ) and low diversity, coinfections by two or more phages are frequent and excess energy availability stimulates inefficient metabolism. Both mechanisms favour phage integration and characterize the Piggyback-the-Winner dynamic. At low densities (below 105 cells ml-1 or g-1 ), starvation represses lytic genes and extends the time window for lysogenic commitment, resulting in a higher frequency of coinfections that cause integration. This pattern follows the predictions of the refugium hypothesis. At intermediary densities (between 105 and 106 cells ml-1 or g-1 ), encounter rates and efficient energy metabolism favour lysis. This may involve Kill-the-Winner lytic dynamics and induction. Based on these three regimes, we propose a framework wherein phage integration occurs more frequently at both ends of the host density gradient, with distinct underlying molecular mechanisms (coinfections and host metabolism) dominating at each extreme.

Multi-Omics Study of Keystone Species in a Cystic Fibrosis Microbiome.

Ecological networking and in vitro studies predict that anaerobic, mucus-degrading bacteria are keystone species in cystic fibrosis (CF) microbiomes. The metabolic byproducts from these bacteria facilitate the colonization and growth of CF pathogens like Pseudomonas aeruginosa. Here, a multi-omics study informed the control of putative anaerobic keystone species during a transition in antibiotic therapy of a CF patient. A quantitative metagenomics approach combining sequence data with epifluorescence microscopy showed that during periods of rapid lung function loss, the patient's lung microbiome was dominated by the anaerobic, mucus-degrading bacteria belonging to Streptococcus, Veillonella, and Prevotella genera. Untargeted metabolomics and community cultures identified high rates of fermentation in these sputa, with the accumulation of lactic acid, citric acid, and acetic acid. P. aeruginosa utilized these fermentation products for growth, as indicated by quantitative transcriptomics data. Transcription levels of P. aeruginosa genes for the utilization of fermentation products were proportional to the abundance of anaerobic bacteria. Clindamycin therapy targeting Gram-positive anaerobes rapidly suppressed anaerobic bacteria and the accumulation of fermentation products. Clindamycin also lowered the abundance and transcription of P. aeruginosa, even though this patient's strain was resistant to this antibiotic. The treatment stabilized the patient's lung function and improved respiratory health for two months, lengthening by a factor of four the between-hospitalization time for this patient. Killing anaerobes indirectly limited the growth of P. aeruginosa by disrupting the cross-feeding of fermentation products. This case study supports the hypothesis that facultative anaerobes operated as keystone species in this CF microbiome. Personalized multi-omics may become a viable approach for routine clinical diagnostics in the future, providing critical information to inform treatment decisions.

Genomic and ecological attributes of marine bacteriophages encoding bacterial virulence genes.

BACKGROUND: Bacteriophages encode genes that modify bacterial functions during infection. The acquisition of phage-encoded virulence genes is a major mechanism for the rise of bacterial pathogens. In coral reefs, high bacterial density and lysogeny has been proposed to exacerbate reef decline through the transfer of phage-encoded virulence genes. However, the functions and distribution of these genes in phage virions on the reef remain unknown. RESULTS: Here, over 28,000 assembled viral genomes from the free viral community in Atlantic and Pacific Ocean coral reefs were queried against a curated database of virulence genes. The diversity of virulence genes encoded in the viral genomes was tested for relationships with host taxonomy and bacterial density in the environment. These analyses showed that bacterial density predicted the profile of virulence genes encoded by phages. The Shannon diversity of virulence-encoding phages was negatively related with bacterial density, leading to dominance of fewer genes at high bacterial abundances. A statistical learning analysis showed that reefs with high microbial density were enriched in viruses encoding genes enabling bacterial recognition and invasion of metazoan epithelium. Over 60% of phages could not have their hosts identified due to limitations of host prediction tools; for those which hosts were identified, host taxonomy was not an indicator of the presence of virulence genes. CONCLUSIONS: This study described bacterial virulence factors encoded in the genomes of bacteriophages at the community level. The results showed that the increase in microbial densities that occurs during coral reef degradation is associated with a change in the genomic repertoire of bacteriophages, specifically in the diversity and distribution of bacterial virulence genes. This suggests that phages are implicated in the rise of pathogens in disturbed marine ecosystems.

Energetic differences between bacterioplankton trophic groups and coral reef resistance.

Coral reefs are among the most productive and diverse marine ecosystems on the Earth. They are also particularly sensitive to changing energetic requirements by different trophic levels. Microbialization specifically refers to the increase in the energetic metabolic demands of microbes relative to macrobes and is significantly correlated with increasing human influence on coral reefs. In this study, metabolic theory of ecology is used to quantify the relative contributions of two broad bacterioplankton groups, autotrophs and heterotrophs, to energy flux on 27 Pacific coral reef ecosystems experiencing human impact to varying degrees. The effective activation energy required for photosynthesis is lower than the average energy of activation for the biochemical reactions of the Krebs cycle, and changes in the proportional abundance of these two groups can greatly affect rates of energy and materials cycling. We show that reef-water communities with a higher proportional abundance of microbial autotrophs expend more metabolic energy per gram of microbial biomass. Increased energy and materials flux through fast energy channels (i.e. water-column associated microbial autotrophs) may dampen the detrimental effects of increased heterotrophic loads (e.g. coral disease) on coral reef systems experiencing anthropogenic disturbance.

Microbial and sponge loops modify fish production in phase-shifting coral reefs.

Shifts from coral to algae dominance of corals reefs have been correlated to fish biomass loss and increased microbial metabolism. Here we investigated reef benthic and planktonic primary production, benthic dissolved organic carbon (DOC) release and bacterial growth efficiency in the Abrolhos Bank, South Atlantic. Benthic DOC release rates are higher while water column bacterial growth efficiency is lower at impacted reefs. A trophic model based on the benthic and planktonic primary production was able to predict the observed relative fish biomass in healthy reefs. In contrast, in impacted reefs, the observed omnivorous fish biomass is higher, while that of the herbivorous/coralivorous fish is lower than predicted by the primary production-based model. Incorporating recycling of benthic-derived carbon in the model through microbial and sponge loops explains the difference and predicts the relative fish biomass in both reef types. Increased benthic carbon release rates and bacterial carbon metabolism, but decreased bacterial growth efficiency could lead to carbon losses through respiration and account for the uncoupling of benthic and fish production in phase-shifting reefs. Carbon recycling by microbial and sponge loops seems to promote an increase of small-bodied fish productivity in phase-shifting coral reefs.

Antibiotic resistance is widespread in urban aquatic environments of Rio de Janeiro, Brazil.

Bacterial resistance to antibiotics has become a public health issue. Over the years, pathogenic organisms with resistance traits have been studied due to the threat they pose to human well-being. However, several studies raised awareness to the often disregarded importance of environmental bacteria as sources of resistance mechanisms. In this work, we analyze the diversity of antibiotic-resistant bacteria occurring in aquatic environments of the state of Rio de Janeiro, Brazil, that are subjected to distinct degrees of anthropogenic impacts. We access the diversity of aquatic bacteria capable of growing in increasing ampicillin concentrations through 16S rRNA gene libraries. This analysis is complemented by the characterization of antibiotic resistance profiles of isolates obtained from urban aquatic environments. We detect communities capable of tolerating antibiotic concentrations up to 600 times higher than the clinical levels. Among the resistant organisms are included potentially pathogenic species, some of them classified as multiresistant. Our results extend the knowledge of the diversity of antibiotic resistance among environmental microorganisms and provide evidence that the diversity of drug-resistant bacteria in aquatic habitats can be influenced by pollution.

Snow viruses and their implications on red snow algal blooms.

Algal blooms can give snowmelt a red color, reducing snow albedo and creating a runaway effect that accelerates snow melting. The occurrence of red snow is predicted to grow in polar and subpolar regions with increasing global temperatures. We hypothesize that these algal blooms affect virus-bacteria interactions in snow, with potential effects on snowmelt dynamics. A genomic analysis of double-stranded DNA virus communities in red and white snow from the Whistler region of British Columbia, Canada, identified 792 putative viruses infecting bacteria. The most abundant putative snow viruses displayed low genomic similarity with known viruses. We recovered the complete circular genomes of nine putative viruses, two of which were classified as temperate. Putative snow viruses encoded genes involved in energy metabolisms, such as NAD+ synthesis and salvage pathways. In model phages, these genes facilitate increased viral particle production and lysis rates. The frequency of temperate phages was positively correlated with microbial abundance in the snow samples. These results suggest the increased frequency of temperate virus-bacteria interactions as microbial densities increase during snowmelt. We propose that this virus-bacteria dynamic may facilitate the red snow algae growth stimulated by bacteria.IMPORTANCEMicrobial communities in red snow algal blooms contribute to intensifying snowmelt rates. The role of viruses in snow during this environmental shift, however, has yet to be elucidated. Here, we characterize novel viruses extracted from snow viral metagenomes and define the functional capacities of snow viruses in both white and red snow. These results are contextualized using the composition and functions observed in the bacterial communities from the same snow samples. Together, these data demonstrate the energy metabolism performed by viruses and bacteria in a snow algal bloom, as well as expand the overall knowledge of viral genomes in extreme environments.

Globally distributed bacteriophage genomes reveal mechanisms of tripartite phage-bacteria-coral interactions.

Reef-building corals depend on an intricate community of microorganisms for functioning and resilience. The infection of coral-associated bacteria by bacteriophages can modify bacteria-host interactions, yet very little is known about phage functions in the holobiont. This gap stems from methodological limitations that have prevented the recovery of high-quality viral genomes and bacterial host assignment from coral samples. Here, we introduce a size fractionation approach that increased bacterial and viral recovery in coral metagenomes by 9-fold and 2-fold, respectively, and enabled the assembly and binning of bacterial and viral genomes at relatively low sequencing coverage. We combined these viral genomes with those derived from 677 publicly available metagenomes, viromes, and bacterial isolates from stony corals to build a global coral virus database of over 20 000 viral genomic sequences spanning four viral realms. The tailed bacteriophage families Kyanoviridae and Autographiviridae were the most abundant, replacing groups formerly referred to as Myoviridae and Podoviridae, respectively. Prophage and CRISPR spacer linkages between these viruses and 626 bacterial metagenome-assembled genomes and bacterial isolates showed that most viruses infected Alphaproteobacteria, the most abundant class, and less abundant taxa like Halanaerobiia and Bacteroidia. A host-phage-gene network identified keystone viruses with the genomic capacity to modulate bacterial metabolic pathways and direct molecular interactions with eukaryotic cells. This study reveals the genomic basis of nested symbioses between bacteriophage, bacteria, and the coral host and its endosymbiotic algae.

The coral microbiome in sickness, in health and in a changing world.

Stony corals, the engines and engineers of reef ecosystems, face unprecedented threats from anthropogenic environmental change. Corals are holobionts that comprise the cnidarian animal host and a diverse community of bacteria, archaea, viruses and eukaryotic microorganisms. Recent research shows that the bacterial microbiome has a pivotal role in coral biology. A healthy bacterial assemblage contributes to nutrient cycling and stress resilience, but pollution, overfishing and climate change can break down these symbiotic relationships, which results in disease, bleaching and, ultimately, coral death. Although progress has been made in characterizing the spatial-temporal diversity of bacteria, we are only beginning to appreciate their functional contribution. In this Review, we summarize the ecological and metabolic interactions between bacteria and other holobiont members, highlight the biotic and abiotic factors influencing the structure of bacterial communities and discuss the impact of climate change on these communities and their coral hosts. We emphasize how microbiome-based interventions can help to decipher key mechanisms underpinning coral health and promote reef resilience. Finally, we explore how recent technological developments may be harnessed to address some of the most pressing challenges in coral microbiology, providing a road map for future research in this field.

Microbial community compositional shifts in bleached colonies of the Brazilian reef-building coral Siderastrea stellata.

The association of metazoan, protist, and microbial communities with Scleractinian corals forms the basis of the coral holobiont. Coral bleaching events have been occurring around the world, introducing changes in the delicate balance of the holobiont symbiotic interactions. In this study, Archaea, bacteria, and eukaryotic phototrophic plastids of bleached colonies of the Brazilian coral Siderastrea stellata were analyzed for the first time, using 16S rRNA gene libraries. Prokaryotic communities were slightly more diverse in healthy than in bleached corals. However, the eukaryotic phototrophic plastids community was more diverse in bleached corals. Archaea phylogenetic analyses revealed a high percentage of Crenarchaeota sequences, mainly related to Nitrosopumilus maritimus and Cenarchaeum symbiosum. Dramatic changes in bacterial community composition were observed in this bleaching episode. The dominant bacterial group was Alphaproteobacteria followed by Gammaproteobacteria in bleached and Betaproteobacteria in healthy samples. Plastid operational taxonomic units (OTUs) from both coral samples were mainly related to red algae chloroplasts (Florideophycea), but we also observed some OTUs related to green algae chloroplasts (Chlorophyta). There seems to be a strong relationship between the Bacillariophyta phylum and our bleached coral samples as clones related to members of the diatom genera Amphora and Nitzschia were detected. The present study reveals information from a poorly investigated coral species and improves the knowledge of coral microbial community shifts that could occur during bleaching episodes.

Water mass age structures the auxiliary metabolic gene content of free-living and particle-attached deep ocean viral communities.

BACKGROUND: Viruses play important roles in the ocean's biogeochemical cycles. Yet, deep ocean viruses are one of the most under-explored fractions of the global biosphere. Little is known about the environmental factors that control the composition and functioning of their communities or how they interact with their free-living or particle-attached microbial hosts. RESULTS: We analysed 58 viral communities associated with size-fractionated free-living (0.2-0.8 µm) and particle-attached (0.8-20 µm) cellular metagenomes from bathypelagic (2150-4018 m deep) microbiomes obtained during the Malaspina expedition. These metagenomes yielded 6631 viral sequences, 91% of which were novel, and 67 represented high-quality genomes. Taxonomic classification assigned 53% of the viral sequences to families of tailed viruses from the order Caudovirales. Computational host prediction associated 886 viral sequences to dominant members of the deep ocean microbiome, such as Alphaproteobacteria (284), Gammaproteobacteria (241), SAR324 (23), Marinisomatota (39), and Chloroflexota (61). Free-living and particle-attached viral communities had markedly distinct taxonomic composition, host prevalence, and auxiliary metabolic gene content, which led to the discovery of novel viral-encoded metabolic genes involved in the folate and nucleotide metabolisms. Water mass age emerged as an important factor driving viral community composition. We postulated this was due to changes in quality and concentration of dissolved organic matter acting on the host communities, leading to an increase of viral auxiliary metabolic genes associated with energy metabolism among older water masses. CONCLUSIONS: These results shed light on the mechanisms by which environmental gradients of deep ocean ecosystems structure the composition and functioning of free-living and particle-attached viral communities. Video Abstract.

Viruses of sulfur oxidizing phototrophs encode genes for pigment, carbon, and sulfur metabolisms.

Viral infections modulate bacterial metabolism and ecology. Here, we investigated the hypothesis that viruses influence the ecology of purple and green sulfur bacteria in anoxic and sulfidic lakes, analogs of euxinic oceans in the geologic past. By screening metagenomes from lake sediments and water column, in addition to publicly-available genomes of cultured purple and green sulfur bacteria, we identified almost 300 high and medium-quality viral genomes. Viruses carrying the gene psbA, encoding the small subunit of photosystem II protein D1, were ubiquitous, suggesting viral interference with the light reactions of sulfur oxidizing autotrophs. Viruses predicted to infect these autotrophs also encoded auxiliary metabolic genes for reductive sulfur assimilation as cysteine, pigment production, and carbon fixation. These observations show that viruses have the genomic potential to modulate the production of metabolic markers of phototrophic sulfur bacteria that are used to identify photic zone euxinia in the geologic past.

Machine learning sheds light on physical-chemical and biological parameters leading to Abrolhos coral reef microbialization.

Microbes play a central role in coral reef health. However, the relative importance of physical-chemical and biological processes in the control of microbial biomass are unknown. Here, we applied machine learning to analyze a large dataset of biological, physical, and chemical parameters (N = 665 coral reef seawater samples) to understand the factors that modulate microbial abundance in the water of Abrolhos reefs, the largest and richest coral reefs of the Southwest Atlantic. Random Forest (RF) and Boosted Regression Tree (BRT) models indicated that hydrodynamic forcing, Dissolved Organic Carbon (DOC), and Total Nitrogen (TN) were the most important predictors of microbial abundance. The possible cumulative effects of higher temperatures, longer seawater residence time, higher nutrient concentration, and lower coral and fish biomass observed in coastal reefs resulted in higher microbial abundance, potentially impacting coral resilience against stressors.

Prophage Genomics and Ecology in the Family Rhodobacteraceae.

Roseobacters are globally abundant bacteria with critical roles in carbon and sulfur biogeochemical cycling. Here, we identified 173 new putative prophages in 79 genomes of Rhodobacteraceae. These prophages represented 1.3 ± 0.15% of the bacterial genomes and had no to low homology with reference and metagenome-assembled viral genomes from aquatic and terrestrial ecosystems. Among the newly identified putative prophages, 35% encoded auxiliary metabolic genes (AMGs), mostly involved in secondary metabolism, amino acid metabolism, and cofactor and vitamin production. The analysis of integration sites and gene homology showed that 22 of the putative prophages were actually gene transfer agents (GTAs) similar to a GTA of Rhodobacter capsulatus. Twenty-three percent of the predicted prophages were observed in the TARA Oceans viromes generated from free viral particles, suggesting that they represent active prophages capable of induction. The distribution of these prophages was significantly associated with latitude and temperature. The prophages most abundant at high latitudes encoded acpP, an auxiliary metabolic gene involved in lipid synthesis and membrane fluidity at low temperatures. Our results show that prophages and gene transfer agents are significant sources of genomic diversity in roseobacter, with potential roles in the ecology of this globally distributed bacterial group.

Nasopharyngeal Microbial Communities of Patients Infected With SARS-CoV-2 That Developed COVID-19.

BACKGROUND: SARS-CoV-2 is an RNA virus causing COVID-19. The clinical characteristics and epidemiology of COVID-19 have been extensively investigated, however, only one study so far focused on the patient's nasopharynx microbiota. In this study we investigated the nasopharynx microbial community of patients that developed different severity levels of COVID-19. We performed 16S ribosomal DNA sequencing from nasopharyngeal swab samples obtained from SARS-CoV-2 positive (56) and negative (18) patients in the province of Alicante (Spain) in their first visit to the hospital. Positive SARS-CoV-2 patients were observed and later categorized in mild (symptomatic without hospitalization), moderate (hospitalization), and severe (admission to ICU). We compared the microbiota diversity and OTU composition among severity groups and built bacterial co-abundance networks for each group. RESULTS: Statistical analysis indicated differences in the nasopharyngeal microbiome of COVID19 patients. 62 OTUs were found exclusively in SARS-CoV-2 positive patients, mostly classified as members of the phylum Bacteroidota (18) and Firmicutes (25). OTUs classified as Prevotella were found to be significantly more abundant in patients that developed more severe COVID-19. Furthermore, co-abundance analysis indicated a loss of network complexity among samples from patients that later developed more severe symptoms. CONCLUSION: Our study shows that the nasopharyngeal microbiome of COVID-19 patients showed differences in the composition of specific OTUs and complexity of co-abundance networks. Taxa with differential abundances among groups could serve as biomarkers for COVID-19 severity. Nevertheless, further studies with larger sample sizes should be conducted to validate these results.

Archaea, Bacteria, and algal plastids associated with the reef-building corals Siderastrea stellata and Mussismilia hispida from Búzios, South Atlantic Ocean, Brazil.

Reef-building corals may be seen as holobiont organisms, presenting diverse associated microbial communities. Best known is the symbiotic relationship with zooxanthellae, but Archaea, Bacteria, fungi, viruses, and algal plastids are also abundant. Until now, there is little information concerning microbial communities associated with Brazilian corals. The present study aims to describe the diversity of Archaea, Bacteria, and eukaryotic algal plastid communities associated with two sympatric species, Siderastrea stellata and Mussismilia hispida, from Southeastern Brazil, using 16S rRNA gene libraries. Since corals present a high number of other associated invertebrates, coral barcoding (COI) was performed to confirm the exclusive occurrence of coral DNA in our samples. Our analysis yielded 354 distinct microbial OTUs, represented mainly by novel phylotypes. Richness (Chao1 and ACE) and diversity (H') estimations of the microbial communities associated with both species were high and comparable to other studies. Rarefaction analyses showed that microbial diversity of S. stellata is higher than that of M. hispida. Libshuff comparative analyses showed that the highest microbial community similarity between the two coral species occurred in the bacterial libraries, while archaeal and plastidial communities were significantly different. Crenarchaeota dominated archaeal communities, while Proteobacteria was the most abundant bacterial phylum, dominated by alpha-Proteobacteria. Plastids were also represented by novel phylotypes and did not match with any 16S rRNA sequences of Cyanobacteria and zooxanthellae from GenBank. Our data improves the pool of available information on Brazilian coral microbes and shows corals as sources of diverse prokaryotic and picoeukaryotic communities.

Quantification of Lysogeny Caused by Phage Coinfections in Microbial Communities from Biophysical Principles.

Temperate phages can associate with their bacterial host to form a lysogen, often modifying the phenotype of the host. Lysogens are dominant in the microbially dense environment of the mammalian gut. This observation contrasts with the long-standing hypothesis of lysogeny being favored at low microbial densities, such as in oligotrophic marine environments. Here, we hypothesized that phage coinfections-a well-understood molecular mechanism of lysogenization-increase at high microbial abundances. To test this hypothesis, we developed a biophysical model of coinfection for marine and gut microbiomes. The model stochastically sampled ranges of phage and bacterial concentrations, adsorption rates, lysogenic commitment times, and community diversity from each environment. In 90% of the sampled marine communities, less than 10% of the bacteria were predicted to be lysogenized via coinfection. In contrast, 25% of the sampled gut communities displayed more than 25% of lysogenization. The probability of lysogenization in the gut was a consequence of the higher densities and higher adsorption rates. These results suggest that, on average, coinfections can form two trillion lysogens in the human gut every day. In marine microbiomes, which were characterized by lower densities and phage adsorption rates, lysogeny via coinfection was still possible for communities with long lysogenic commitment times. Our study indicates that different physical factors causing coinfections can reconcile the traditional view of lysogeny at poor host growth (long commitment times) and the recent Piggyback-the-Winner framework proposing that lysogeny is favored in rich environments (high densities and adsorption rates).IMPORTANCE The association of temperate phages and bacterial hosts during lysogeny manipulates microbial dynamics from the oceans to the human gut. Lysogeny is well studied in laboratory models, but its environmental drivers remain unclear. Here, we quantified the probability of lysogenization caused by phage coinfections, a well-known trigger of lysogeny, in marine and gut microbial environments. Coinfections were quantified by developing a biophysical model that incorporated the traits of viral and bacterial communities. Lysogenization via coinfection was more frequent in highly productive environments like the gut, due to higher microbial densities and higher phage adsorption rates. At low cell densities, lysogenization occurred in bacteria with long duplication times. These results bridge the molecular understanding of lysogeny with the ecology of complex microbial communities.

Archaeal and bacterial communities of heavy metal contaminated acidic waters from zinc mine residues in Sepetiba Bay.

Mining of metallic sulfide ore produces acidic water with high metal concentrations that have harmful consequences for aquatic life. To understand the composition and structure of microbial communities in acid mine drainage (AMD) waters associated with Zn mine tailings, molecular diversity of 16S genes was examined using a PCR, cloning, and sequencing approach. A total of 78 operational taxonomic units (OTUs) were obtained from samples collected at five different sites in and around mining residues in Sepetiba Bay, Brazil. We analyzed metal concentration, physical, chemical, and microbiological parameters related to prokaryotic diversity in low metal impacted compared to highly polluted environments with Zn at level of gram per liter and Cd-Pb at level of microgram per liter. Application of molecular methods for community structure analyses showed that Archaea and Bacteria groups present a phylogenetic relationship with uncultured environmental organisms. Phylogenetic analysis revealed that bacteria present at the five sites fell into seven known divisions, alpha-Proteobacteria (13.4%), beta-Proteobacteria (16.3%), gamma-Proteobacteria (4.3%), Sphingobacteriales (4.3%), Actinobacteria (3.2%) Acidobacteria (2.1%), Cyanobacteria (11.9%), and unclassified bacteria (44.5%). Almost all archaeal clones were related to uncultivated Crenarchaeota species, which were shared between high impacted and low impacted waters. Rarefaction curves showed that bacterial groups are more diverse than archaeal groups while the overall prokaryotic biodiversity is lower in high metal impacted environments than in less polluted habitats. Knowledge of this microbial community structure will help in understanding prokaryotic diversity, biogeography, and the role of microorganisms in zinc smelting AMD generation and perhaps it may be exploited for environmental remediation procedures in this area.