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1.
BMC Biol ; 21(1): 77, 2023 04 11.
Artigo em Inglês | MEDLINE | ID: mdl-37038111

RESUMO

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.


Assuntos
Antozoários , Bactérias , Recifes de Corais , Peixes , Cadeia Alimentar , Comportamento Predatório , Antozoários/microbiologia , Antozoários/virologia , Animais , Peixes/fisiologia , Oceano Pacífico , Biomassa , Ilhas , Bactérias/virologia , Água do Mar/química , Atividades Humanas , Estatísticas não Paramétricas
2.
Environ Microbiol ; 21(6): 2182-2197, 2019 06.
Artigo em Inglês | MEDLINE | ID: mdl-31001863

RESUMO

Coccolithoviruses (EhVs) are large, double-stranded DNA-containing viruses that infect the single-celled, marine coccolithophore Emiliania huxleyi. Given the cosmopolitan nature and global importance of E. huxleyi as a bloom-forming, calcifying, photoautotroph, E. huxleyi-EhV interactions play a key role in oceanic carbon biogeochemistry. Virally-encoded glycosphingolipids (vGSLs) are virulence factors that are produced by the activity of virus-encoded serine palmitoyltransferase (SPT). Here, we characterize the dynamics, diversity and catalytic production of vGSLs in an array of EhV strains in relation to their SPT sequence composition and explore the hypothesis that they are a determinant of infectivity and host demise. vGSL production and diversity was positively correlated with increased virulence, virus replication rate and lytic infection dynamics in laboratory experiments, but they do not explain the success of less-virulent EhVs in natural EhV communities. The majority of EhV-derived SPT amplicon sequences associated with infected cells in the North Atlantic derived from slower infecting, less virulent EhVs. Our lab-, field- and mathematical model-based data and simulations support ecological scenarios whereby slow-infecting, less-virulent EhVs successfully compete in North Atlantic populations of E. huxleyi, through either the preferential removal of fast-infecting, virulent EhVs during active infection or by having access to a broader host range.


Assuntos
Glicoesfingolipídeos/biossíntese , Phycodnaviridae/metabolismo , Ecologia , Haptófitas/virologia , Modelos Teóricos , Phycodnaviridae/enzimologia , Phycodnaviridae/genética , Phycodnaviridae/patogenicidade , Serina C-Palmitoiltransferase , Proteínas Virais/genética , Proteínas Virais/metabolismo , Virulência , Replicação Viral
3.
New Phytol ; 221(3): 1289-1302, 2019 02.
Artigo em Inglês | MEDLINE | ID: mdl-30368816

RESUMO

Viruses that infect photoautotrophs have a fundamental relationship with light, given the need for host resources. We investigated the role of light on Coccolithovirus (EhV) infection of the globally distributed coccolithophore, Emiliania huxleyi. Light was required for EhV adsorption, and viral production was highest when host cultures were maintained in continuous light or at irradiance levels of 150-300 µmol m-2  s-1 . During the early stages of infection, photosynthetic electron transport remained high, while RuBisCO expression decreased concomitant with an induction of the pentose phosphate pathway, the primary source of de novo nucleotides. A mathematical model developed and fitted to the laboratory data supported the hypothesis that EhV replication was controlled by a trade-off between host nucleotide recycling and de novo synthesis, and that photoperiod and photon flux could toggle this switch. Laboratory results supported field observations that light was the most robust driver of EhV replication within E. huxleyi populations collected across a 2000 nautical mile transect in the North Atlantic. Collectively, these findings demonstrate that light can drive host-virus interactions through a mechanistic interplay between host metabolic processes, which serve to structure infection and phytoplankton mortality in the upper ocean.


Assuntos
Haptófitas/efeitos da radiação , Haptófitas/virologia , Interações Hospedeiro-Patógeno/efeitos da radiação , Luz , Phycodnaviridae/fisiologia , Adsorção , Haptófitas/crescimento & desenvolvimento , NADP/metabolismo , Nucleotídeos/biossíntese , Via de Pentose Fosfato/efeitos da radiação , Fotoperíodo , Fotossíntese/efeitos da radiação
4.
Nature ; 549(7672): E3-E4, 2017 09 20.
Artigo em Inglês | MEDLINE | ID: mdl-28933437
5.
Environ Microbiol ; 17(12): 5100-8, 2015 Dec.
Artigo em Inglês | MEDLINE | ID: mdl-26310718

RESUMO

Marine photosynthesis is largely driven by cyanobacteria, namely Synechococcus and Prochlorococcus. Genes encoding for photosystem (PS) I and II reaction centre proteins are found in cyanophages and are believed to increase their fitness. Two viral PSI gene arrangements are known, psaJF→C→A→B→K→E→D and psaD→C→A→B. The shared genes between these gene cassettes and their encoded proteins are distinguished by %G + C and protein sequence respectively. The data on the psaD→C→A→B gene organization were reported from only two partial gene cassettes coming from Global Ocean Sampling stations in the Pacific and Indian oceans. Now we have extended our search to 370 marine stations from six metagenomic projects. Genes corresponding to both PSI gene arrangements were detected in the Pacific, Indian and Atlantic oceans, confined to a strip along the equator (30°N and 30°S). In addition, we found that the predicted structure of the viral PsaA protein from the psaD→C→A→B organization contains a lumenal loop conserved in PsaA proteins from Synechococcus, but is completely absent in viral PsaA proteins from the psaJF→C→A→B→K→E→D gene organization and most Prochlorococcus strains. This may indicate a co-evolutionary scenario where cyanophages containing either of these gene organizations infect cyanobacterial ecotypes biogeographically restricted to the 30°N and 30°S equatorial strip.


Assuntos
Bacteriófagos/genética , Fotossíntese/genética , Complexo de Proteína do Fotossistema I/genética , Prochlorococcus/genética , Synechococcus/genética , Sequência de Aminoácidos , Organismos Aquáticos/genética , Organismos Aquáticos/metabolismo , Oceano Atlântico , Evolução Biológica , Ordem dos Genes , Genes Virais/genética , Oceano Índico , Metagenômica , Oceano Pacífico , Complexo de Proteína do Fotossistema II/genética , Prochlorococcus/metabolismo , Prochlorococcus/virologia , Synechococcus/metabolismo , Synechococcus/virologia
6.
PLoS One ; 18(7): e0288114, 2023.
Artigo em Inglês | MEDLINE | ID: mdl-37418487

RESUMO

Viral lysis of phytoplankton is one of the most common forms of death on Earth. Building on an assay used extensively to assess rates of phytoplankton loss to predation by grazers, lysis rates are increasingly quantified through dilution-based techniques. In this approach, dilution of viruses and hosts are expected to reduce infection rates and thus increase host net growth rates (i.e., accumulation rates). The difference between diluted and undiluted host growth rates is interpreted as a measurable proxy for the rate of viral lytic death. These assays are usually conducted in volumes ≥ 1 L. To increase throughput, we implemented a miniaturized, high-throughput, high-replication, flow cytometric microplate dilution assay to measure viral lysis in environmental samples sourced from a suburban pond and the North Atlantic Ocean. The most notable outcome we observed was a decline in phytoplankton densities that was exacerbated by dilution, instead of the increased growth rates expected from lowered virus-phytoplankton encounters. We sought to explain this counterintuitive outcome using theoretical, environmental, and experimental analyses. Our study shows that, while die-offs could be partly explained by a 'plate effect' due to small incubation volumes and cells adhering to walls, the declines in phytoplankton densities are not volume-dependent. Rather, they are driven by many density- and physiology-dependent effects of dilution on predation pressure, nutrient limitation, and growth, all of which violate the original assumptions of dilution assays. As these effects are volume-independent, these processes likely occur in all dilution assays that our analyses show to be remarkably sensitive to dilution-altered phytoplankton growth and insensitive to actual predation pressure. Incorporating altered growth as well as predation, we present a logical framework that categorizes locations by the relative dominance of these mechanisms, with general applicability to dilution-based assays.


Assuntos
Comportamento Predatório , Vírus , Animais , Fitoplâncton , Oceano Atlântico , Lagoas
7.
Nat Commun ; 12(1): 6634, 2021 11 17.
Artigo em Inglês | MEDLINE | ID: mdl-34789722

RESUMO

Seasonal shifts in phytoplankton accumulation and loss largely follow changes in mixed layer depth, but the impact of mixed layer depth on cell physiology remains unexplored. Here, we investigate the physiological state of phytoplankton populations associated with distinct bloom phases and mixing regimes in the North Atlantic. Stratification and deep mixing alter community physiology and viral production, effectively shaping accumulation rates. Communities in relatively deep, early-spring mixed layers are characterized by low levels of stress and high accumulation rates, while those in the recently shallowed mixed layers in late-spring have high levels of oxidative stress. Prolonged stratification into early autumn manifests in negative accumulation rates, along with pronounced signatures of compromised membranes, death-related protease activity, virus production, nutrient drawdown, and lipid markers indicative of nutrient stress. Positive accumulation renews during mixed layer deepening with transition into winter, concomitant with enhanced nutrient supply and lessened viral pressure.


Assuntos
Fitoplâncton/fisiologia , Fitoplâncton/virologia , Água do Mar/microbiologia , Oceano Atlântico , Biomassa , Eutrofização , Estações do Ano , Água do Mar/química , Estresse Fisiológico , Fenômenos Fisiológicos Virais
8.
Gut Microbes ; 11(4): 721-734, 2020 07 03.
Artigo em Inglês | MEDLINE | ID: mdl-31931655

RESUMO

The approximately 1011 viruses and microbial cells per gram of fecal matter (dry weight) in the large intestine are important to human health. The responses of three common gut bacteria species, and one opportunistic pathogen, to 117 commonly consumed foods, chemical additives, and plant extracts were tested. Many compounds, including Stevia rebaudiana and bee propolis extracts, exhibited species-specific growth inhibition by prophage induction. Overall, these results show that various foods may change the abundances of gut bacteria by modulating temperate phage and suggests a novel path for landscaping the human gut microbiome.


Assuntos
Antibacterianos/farmacologia , Bactérias/crescimento & desenvolvimento , Alimentos , Microbioma Gastrointestinal , Extratos Vegetais/farmacologia , Ativação Viral , Bactérias/efeitos dos fármacos , Dieta , Fezes/microbiologia , Aditivos Alimentares/farmacologia , Humanos , Metagenoma
9.
Nat Commun ; 11(1): 4626, 2020 09 15.
Artigo em Inglês | MEDLINE | ID: mdl-32934228

RESUMO

The blooming cosmopolitan coccolithophore Emiliania huxleyi and its viruses (EhVs) are a model for density-dependent virulent dynamics. EhVs commonly exhibit rapid viral reproduction and drive host death in high-density laboratory cultures and mesocosms that simulate blooms. Here we show that this system exhibits physiology-dependent temperate dynamics at environmentally relevant E. huxleyi host densities rather than virulent dynamics, with viruses switching from a long-term non-lethal temperate phase in healthy hosts to a lethal lytic stage as host cells become physiologically stressed. Using this system as a model for temperate infection dynamics, we present a template to diagnose temperate infection in other virus-host systems by integrating experimental, theoretical, and environmental approaches. Finding temperate dynamics in such an established virulent host-virus model system indicates that temperateness may be more pervasive than previously considered, and that the role of viruses in bloom formation and decline may be governed by host physiology rather than by host-virus densities.


Assuntos
Haptófitas/virologia , Vírus de Plantas/fisiologia , Vírus de Plantas/patogenicidade , Haptófitas/fisiologia , Interações Hospedeiro-Patógeno , Modelos Biológicos , Virulência
10.
PeerJ ; 5: e3423, 2017.
Artigo em Inglês | MEDLINE | ID: mdl-28649468

RESUMO

Human impacts are causing ecosystem phase shifts from coral- to algal-dominated reef systems on a global scale. As these ecosystems undergo transition, there is an increased incidence of coral-macroalgal interactions. Mounting evidence indicates that the outcome of these interaction events is, in part, governed by microbially mediated dynamics. The allocation of available energy through different trophic levels, including the microbial food web, determines the outcome of these interactions and ultimately shapes the benthic community structure. However, little is known about the underlying thermodynamic mechanisms involved in these trophic energy transfers. This study utilizes a novel combination of methods including calorimetry, flow cytometry, and optical oxygen measurements, to provide a bioenergetic analysis of coral-macroalgal interactions in a controlled aquarium setting. We demonstrate that the energetic demands of microbial communities at the coral-algal interaction interface are higher than in the communities associated with either of the macroorganisms alone. This was evident through higher microbial power output (energy use per unit time) and lower oxygen concentrations at interaction zones compared to areas distal from the interface. Increases in microbial power output and lower oxygen concentrations were significantly correlated with the ratio of heterotrophic to autotrophic microbes but not the total microbial abundance. These results suggest that coral-algal interfaces harbor higher proportions of heterotrophic microbes that are optimizing maximal power output, as opposed to yield. This yield to power shift offers a possible thermodynamic mechanism underlying the transition from coral- to algal-dominated reef ecosystems currently being observed worldwide. As changes in the power output of an ecosystem are a significant indicator of the current state of the system, this analysis provides a novel and insightful means to quantify microbial impacts on reef health.

11.
Nat Microbiol ; 2: 17064, 2017 Apr 28.
Artigo em Inglês | MEDLINE | ID: mdl-28452987

RESUMO

Temperate bacterial viruses (phages) may enter a symbiosis with their host cell, forming a unit called a lysogen. Infection and viral replication are disassociated in lysogens until an induction event such as DNA damage occurs, triggering viral-mediated lysis. The lysogen-lytic viral reproduction switch is central to viral ecology, with diverse ecosystem impacts. It has been argued that lysogeny is favoured in phages at low host densities. This paradigm is based on the fraction of chemically inducible cells (FCIC) lysogeny proxy determined using DNA-damaging mitomycin C inductions. Contrary to the established paradigm, a survey of 39 inductions publications found FCIC to be highly variable and pervasively insensitive to bacterial host density at global, within-environment and within-study levels. Attempts to determine the source(s) of variability highlighted the inherent complications in using the FCIC proxy in mixed communities, including dissociation between rates of lysogeny and FCIC values. Ultimately, FCIC studies do not provide robust measures of lysogeny or consistent evidence of either positive or negative host density dependence to the lytic-lysogenic switch. Other metrics are therefore needed to understand the drivers of the lytic-lysogenic decision in viral communities and to test models of the host density-dependent viral lytic-lysogenic switch.


Assuntos
Bactérias/virologia , Bacteriófagos/fisiologia , Lisogenia , Bacteriófagos/genética , Dano ao DNA , Ecossistema , Meio Ambiente , Simbiose , Replicação Viral
12.
Nat Microbiol ; 1(6): 16042, 2016 04 25.
Artigo em Inglês | MEDLINE | ID: mdl-27572833

RESUMO

Microbialization refers to the observed shift in ecosystem trophic structure towards higher microbial biomass and energy use. On coral reefs, the proximal causes of microbialization are overfishing and eutrophication, both of which facilitate enhanced growth of fleshy algae, conferring a competitive advantage over calcifying corals and coralline algae. The proposed mechanism for this competitive advantage is the DDAM positive feedback loop (dissolved organic carbon (DOC), disease, algae, microorganism), where DOC released by ungrazed fleshy algae supports copiotrophic, potentially pathogenic bacterial communities, ultimately harming corals and maintaining algal competitive dominance. Using an unprecedented data set of >400 samples from 60 coral reef sites, we show that the central DDAM predictions are consistent across three ocean basins. Reef algal cover is positively correlated with lower concentrations of DOC and higher microbial abundances. On turf and fleshy macroalgal-rich reefs, higher relative abundances of copiotrophic microbial taxa were identified. These microbial communities shift their metabolic potential for carbohydrate degradation from the more energy efficient Embden-Meyerhof-Parnas pathway on coral-dominated reefs to the less efficient Entner-Doudoroff and pentose phosphate pathways on algal-dominated reefs. This 'yield-to-power' switch by microorganism directly threatens reefs via increased hypoxia and greater CO2 release from the microbial respiration of DOC.


Assuntos
Antozoários/crescimento & desenvolvimento , Bactérias/crescimento & desenvolvimento , Biomassa , Recifes de Corais , Alga Marinha/crescimento & desenvolvimento , Alga Marinha/metabolismo , Animais , Antozoários/metabolismo , Bactérias/metabolismo , Metabolismo dos Carboidratos , Carbono/metabolismo , Ciclo do Carbono , Eutrofização , Glicólise , Via de Pentose Fosfato
13.
J Vis Exp ; (93): e52131, 2014 Nov 05.
Artigo em Inglês | MEDLINE | ID: mdl-25407983

RESUMO

Here we introduce a series of thoroughly tested and well standardized research protocols adapted for use in remote marine environments. The sampling protocols include the assessment of resources available to the microbial community (dissolved organic carbon, particulate organic matter, inorganic nutrients), and a comprehensive description of the viral and bacterial communities (via direct viral and microbial counts, enumeration of autofluorescent microbes, and construction of viral and microbial metagenomes). We use a combination of methods, which represent a dispersed field of scientific disciplines comprising already established protocols and some of the most recent techniques developed. Especially metagenomic sequencing techniques used for viral and bacterial community characterization, have been established only in recent years, and are thus still subjected to constant improvement. This has led to a variety of sampling and sample processing procedures currently in use. The set of methods presented here provides an up to date approach to collect and process environmental samples. Parameters addressed with these protocols yield the minimum on information essential to characterize and understand the underlying mechanisms of viral and microbial community dynamics. It gives easy to follow guidelines to conduct comprehensive surveys and discusses critical steps and potential caveats pertinent to each technique.


Assuntos
Metagenômica/métodos , Água do Mar/química , Água do Mar/microbiologia , Microbiologia da Água , Bactérias/genética , Ecossistema , Metagenoma , Oceanos e Mares , Vírus/genética
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