scholarly journals Viral infection of algal blooms leaves a unique metabolic footprint on the dissolved organic matter in the ocean

2021 ◽  
Vol 7 (25) ◽  
pp. eabf4680
Author(s):  
Constanze Kuhlisch ◽  
Guy Schleyer ◽  
Nir Shahaf ◽  
Flora Vincent ◽  
Daniella Schatz ◽  
...  
Keyword(s):  
Organic Matter ◽  
Dissolved Organic Matter ◽  
Primary Production ◽  
Viral Infection ◽  
Algal Blooms ◽  
Trophic Levels ◽  
Dynamic Changes ◽  
Marine Food Web ◽  
Key Players ◽  
Marine Food

Algal blooms are hotspots of primary production in the ocean, forming the basis of the marine food web and fueling the dissolved organic matter (DOM) pool. Viruses are key players in controlling algal demise, thereby diverting biomass from higher trophic levels to the DOM pool, a process termed the “viral shunt.” To decode the metabolic footprint of the viral shunt in the environment, we induced a bloom of Emiliania huxleyi and followed its succession using untargeted exometabolomics. We show that bloom succession induces dynamic changes in the exometabolic landscape. We found a set of chlorine-iodine–containing metabolites that were induced by viral infection and released during bloom demise. These metabolites were further detected in virus-infected oceanic E. huxleyi blooms. Therefore, we propose that halogenation with both chlorine and iodine is a distinct hallmark of the virus-induced DOM of E. huxleyi, providing insights into the metabolic consequences of the viral shunt.

scholarly journals Viral infection of algal blooms leaves a halogenated footprint on the dissolved organic matter in the ocean

2020 ◽  
Author(s):  
Constanze Kuhlisch ◽  
Guy Schleyer ◽  
Nir Shahaf ◽  
Flora Vincent ◽  
Daniella Schatz ◽  
...  
Keyword(s):  
Organic Matter ◽  
Dissolved Organic Matter ◽  
Viral Infection ◽  
Natural Environment ◽  
Algal Blooms ◽  
Algal Bloom ◽  
Trophic Levels ◽  
Viral Gene ◽  
Gene Marker ◽  
Market Place

AbstractAlgal blooms are important hotspots of primary production in the ocean, forming the basis of the marine food web and fueling the pool of dissolved organic matter (DOM)1, which is the largest global inventory of reduced carbon and a market place for metabolic exchange in the ocean2. Marine viruses are key players in controlling algal bloom demise and act as major biogeochemical drivers of nutrient cycling and metabolic fluxes by shunting algal biomass from higher trophic levels to the DOM pool, a process termed the ‘viral shunt’3,4. Nevertheless, the metabolic composition of virus-induced DOM (vDOM) in the marine environment is unknown. To decode the metabolic footprint of the ‘viral shunt’, we induced a bloom of the ecologically important alga Emiliania huxleyi in the natural environment, and followed its succession using an untargeted exometabolomics approach. Here we show that algal bloom succession induces extensive and dynamic changes in the exometabolic landscape, especially during bloom demise. By correlating to a specific viral gene marker, we discovered a set of novel chlorine-iodine-containing metabolites that were induced by viral infection and copiously released during bloom demise. We further detected several of these chloro-iodo metabolites in virus-infected open ocean blooms of E. huxleyi, supporting their use as sensitive biomarkers for virus-induced demise in the natural environment. Therefore, we propose halogenation to be a hallmark of the E. huxleyi vDOM, providing insights into the profound metabolic consequences of viral infection for the marine DOM pool.

scholarly journals Viral lysis alters the optical properties and biological availability of dissolved organic matter derived from picocyanobacteria Prochlorococcus

2020 ◽  
Author(s):  
Xilin Xiao ◽  
Weidong Guo ◽  
Xiaolin Li ◽  
Chao Wang ◽  
Xiaowei Chen ◽  
...  
Keyword(s):  
Organic Matter ◽  
Optical Properties ◽  
Bacterial Community ◽  
Dissolved Organic Matter ◽  
Primary Production ◽  
Viral Infection ◽  
Biological Availability ◽  
Absorption Coefficients ◽  
Viral Lysis ◽  
Microbial Utilization

Phytoplankton contribute almost half of the world's total primary production. The exudates and viral lysates of phytoplankton are two important forms of dissolved organic matter (DOM) in aquatic environments and fuel heterotrophic prokaryotic metabolism. However, the effect of viral infection on the composition and biological availability of phytoplankton-released DOM is poorly understood. Here, we investigated the optical characteristics and microbial utilization of the exudates and viral lysates of the ecologically important unicellular picophytoplankton Prochlorococcus. Our results showed that Prochlorococcus DOM produced by viral lysis (Pro-vDOM) with phages of three different morphotypes (myovirus P-HM2, siphovirus P-HS2 and podovirus P-SSP7) had higher humic-like fluorescence intensities, lower absorption coefficients and higher spectral slopes compared to DOM exuded by Prochlorococcus (Pro-exudate). The results indicate that viral infection altered the composition of Prochlorococcus-derived DOM and might contribute to the pool of oceanic humic-like DOM. Incubation with Pro-vDOM resulted in a greater dissolved organic carbon (DOC) degradation rate and decreases in the absorption spectral slope and heterotrophic bacterial growth rate compared to incubation with Pro-exudate, suggesting that Pro-vDOM was more bioavailable compared to Pro-exudate. In addition, the stimulated microbial community succession trajectories were significantly different between the Pro-exudate and Pro-vDOM treatments, indicating that viral lysates play an important role in shaping the heterotrophic bacterial community. Our study demonstrated that viral lysis altered the chemical composition and biological availability of DOM derived from Prochlorococcus, which is the numerically dominant phytoplankton in the oligotrophic ocean. Importance The unicellular picocyanobacterium Prochlorococcus is the numerically dominate phytoplankton in the oligotrophic ocean, contributing to the vast majority of marine primary production. Prochlorococcus releases a significant fraction of fixed organic matter into surrounding environment and supports a vital portion of heterotrophic bacterial activity. Viral lysis is an important biomass loss process of Prochlorococcus. Yet little is known about whether and how viral lysis affects Prochlorococcus-released dissolved organic matter (DOM). Our paper shows that viral infection alters the optical properties (such as the absorption coefficients, spectral slopes and fluorescence intensities) of released DOM and might contribute to a humic-like DOM pool and carbon sequestration in the ocean. Meanwhile, viral lysis also releases various intracellular labile DOM including amino acids, protein-like DOM and lower-molecular weight DOM, increases the bioavailability of DOM and shapes the successive trajectory of the heterotrophic bacterial community. Our study highlights the importance of viruses in impacting the DOM quality in the ocean.

scholarly journals Viral infection switches the balance between bacterial and eukaryotic recyclers of organic matter during algal blooms

2021 ◽  
Author(s):  
Flora Vincent ◽  
Matti Gralka ◽  
Guy Schleyer ◽  
Daniella J Schatz ◽  
Miguel Cabrera-Brudau ◽  
...  
Keyword(s):  
Organic Matter ◽  
Viral Infection ◽  
Algal Blooms ◽  
Large Scale ◽  
Deep Ocean ◽  
Trophic Levels ◽  
Microbiome Composition ◽  
Carbon Release ◽  
Open Question ◽  
The Impact

Algal blooms are hotspots of marine primary production and play central roles in microbial ecology and global nutrient cycling. When blooms collapse, organic carbon is transferred to higher trophic levels, microbial respiration or sinking in proportions that depend on the dominant mortality agent. Viral infection can lead to bloom termination, but its impact on the fate of carbon remains an open question. Here, we characterized the consequences of viral infection on the microbiome composition and biogeochemical landscape of marine ecosystems by conducting a large-scale mesocosm experiment. Moniroting of seven induced coccolithophore blooms, which showed different degrees of viral infection, revealed that only high levels of viral infection caused significant shifts in the composition of free-living bacterial and eukaryotic assemblages. Intriguingly, viral infection favored the growth of eukaryotic heterotrophs (thraustochytrids) over bacteria as potential recyclers of organic matter. By combining modeling and quantification of active viral infection at a single-cell resolution, we estimate that viral infection can increase per-cell rates of extracellular carbon release by 2-4.5 fold. This happened via production of acidic polysaccharides and particulate inorganic carbon, two major contributors to carbon sinking into the deep ocean. These results reveal the impact of viral infection on the fate of carbon through microbial recyclers of organic matter in large-scale coccolithophore blooms.

scholarly journals Viral infection switches the balance between bacterial and eukaryotic recyclers of organic matter during algal blooms

2021 ◽  
Author(s):  
Flora VINCENT ◽  
Matti Gralka ◽  
Guy Schleyer ◽  
Daniella Schatz ◽  
Miguel Cabrera-Brufau ◽  
...  
Keyword(s):  
Organic Matter ◽  
Viral Infection ◽  
Algal Blooms ◽  
Large Scale ◽  
Deep Ocean ◽  
Trophic Levels ◽  
Microbiome Composition ◽  
Carbon Release ◽  
Open Question ◽  
The Impact

Abstract Algal blooms are hotspots of marine primary production and play central roles in microbial ecology and global nutrient cycling. When blooms collapse, organic carbon is transferred to higher trophic levels, microbial respiration or sinking in proportions that depend on the dominant mortality agent. Viral infection can lead to bloom termination, but its impact on the fate of carbon remains an open question. Here, we characterized the consequences of viral infection on the microbiome composition and biogeochemical landscape of marine ecosystems by conducting a large-scale mesocosm experiment. Moniroting of seven induced coccolithophore blooms, which showed different degrees of viral infection, revealed that only high levels of viral infection caused significant shifts in the composition of free-living bacterial and eukaryotic assemblages. Intriguingly, viral infection favored the growth of eukaryotic heterotrophs (thraustochytrids) over bacteria as potential recyclers of organic matter. By combining modeling and quantification of active viral infection at a single-cell resolution, we estimate that viral infection can increase per-cell rates of extracellular carbon release by 2-4.5 fold. This happened via production of acidic polysaccharides and particulate inorganic carbon, two major contributors to carbon sinking into the deep ocean. These results reveal the impact of viral infection on the fate of carbon through microbial recyclers of organic matter in large-scale coccolithophore blooms.

scholarly journals Sink or link? The bacterial role in benthic carbon cycling in the Arabian Sea's oxygen minimum zone

2013 ◽  
Vol 10 (11) ◽  
pp. 6879-6891 ◽  
Author(s):  
L. Pozzato ◽  
D. Van Oevelen ◽  
L. Moodley ◽  
K. Soetaert ◽  
J. J. Middelburg
Keyword(s):  
Organic Matter ◽  
Dissolved Organic Matter ◽  
Particulate Organic Matter ◽  
Experimental Period ◽  
Oxygen Minimum Zone ◽  
Trophic Levels ◽  
Isotope Tracer ◽  
Oxygen Conditions ◽  
Minimum Zone ◽  
Oxygen Minimum

Abstract. The bacterial loop, the consumption of dissolved organic matter (DOM) by bacteria and subsequent transfer of bacterial carbon to higher trophic levels, plays a prominent role in pelagic food webs. However, its role in sedimentary ecosystems is not well documented. Here we present the results of isotope tracer experiments performed under in situ oxygen conditions in sediments from inside and outside the Arabian Sea's oxygen minimum zone (OMZ) to study the importance of the microbial loop in this setting. Particulate organic matter, added as phytodetritus, was processed by bacteria, protozoa and metazoans, while dissolved organic matter was processed only by bacteria and there was very little, if any, transfer to higher trophic levels within the 7 day experimental period. This lack of significant transfer of bacterial-derived carbon to metazoan consumers indicates that the bacterial loop is rather inefficient, in sediments both inside and outside the OMZ. Moreover, metazoans directly consumed labile particulate organic matter resources and thus competed with bacteria for phytodetritus.

scholarly journals Linkage between the temporal and spatial variability of dissolved organic matter and whole-stream metabolism

2013 ◽  
Vol 10 (8) ◽  
pp. 5555-5569 ◽  
Author(s):  
S. Halbedel ◽  
O. Büttner ◽  
M. Weitere
Keyword(s):  
Molecular Weight ◽  
Organic Matter ◽  
Dissolved Organic Matter ◽  
Primary Production ◽  
Gross Primary Production ◽  
Complex Structure ◽  
Low Molecular Weight ◽  
Stream Metabolism ◽  
Temporal And Spatial ◽  
Dom Composition

Abstract. Dissolved organic matter (DOM) is an important resource for microbes, thus affecting whole-stream metabolism. However, the factors influencing its chemical composition and thereby also its bio-availability are complex and not thoroughly understood. It was hypothesized that whole-stream metabolism is linked to DOM composition and that the coupling of both is influenced by seasonality and different land-use types. We tested this hypothesis in a comparative study on two pristine forestry streams and two non-forestry streams. The investigated streams were located in the Harz Mountains (central Europe, Germany). The metabolic rate was measured with a classical two-station oxygen change technique and the variability of DOM with fluorescence spectroscopy. All streams were clearly net heterotrophic, whereby non-forestry streams showed a higher primary production, which was correlated to irradiance and phosphorus concentration. We detected three CDOM components (C1, C2, C3) using parallel factor (PARAFAC) analysis. We compared the excitation and emission maxima of these components with the literature and correlated the PARAFAC components with each other and with fluorescence indices. The correlations suggest that two PARAFAC components are derived from allochthonous sources (C1, C3) and one is derived autochthonously (C2). The chromophoric DOM matrix was dominated by signals of humic-like substances with a highly complex structure, followed by humic-like, fulfic acids, low-molecular-weight substances, and with minor amounts of amino acids and proteins. The ratios of these PARAFAC components (C1 : C2, C1 : C3, C3 : C2) differed with respect to stream types (forestry versus non-forestry). We demonstrated a significant correlation between gross primary production (GPP) and signals of autochthonously derived, low-molecular-weight humic-like substances. A positive correlation between P / R (i.e. GPP/daily community respiration) and the fluorescence index FI suggests that the amount of autochthonously produced DOM increased overall with increasing GPP. In accordance with the coupling between DOM and the metabolism, our data also indicate that the composition of DOM is subject to seasonal fluctuations. We concluded that temporal and spatial differences in DOM composition are driven by whole-stream metabolism, in addition to pronounced effects coming from allochthonous sources.

Modern methane and dissolved organic matter radiocarbon signatures suggest rapid transfer of organic carbon from a tropical forest to the underlying subterranean estuary ecosystem

2020 ◽  
Author(s):  
David Brankovits ◽  
John Pohlman ◽  
Mark Garnett ◽  
Joshua Dean
Keyword(s):  
Organic Matter ◽  
Organic Carbon ◽  
Dissolved Organic Matter ◽  
Food Web ◽  
Land Surface ◽  
Dissolved Inorganic Carbon ◽  
Trophic Levels ◽  
Carbon Turnover ◽  
Isotopic Analyses ◽  
Subterranean Estuaries

<p>Biogeochemical processing of dissolved organic matter, including methane, along sharp salinity gradients in subterranean estuaries greatly alters the composition of submarine groundwater discharge into the marine environment. Along the margins of coastal carbonate (karst) platforms, which account for ~25% of all coastlines, subterranean estuaries extend kilometers inland within porous bedrock, flooding extensive cave networks. This environment harbors a poorly understood, but globally dispersed, anchialine fauna (invertebrates with subterranean adaptations) and characteristic microbial communities. In Mexico’s Yucatan Peninsula, microbial processing of methane and dissolved organic carbon (DOC), originating from overlying tropical soils, is the critical link for shuttling organic matter to higher trophic levels of the food web within the coastal aquifer. To better understand carbon turnover during organic matter transformations in this habitat, we collected samples for stable and radiocarbon analyses targeting the biotic and abiotic components of the carbon cycle. In the freshwater, radiocarbon signatures of terrestrially originated DOC (pMC = 105.1; [DOC] = 517 µM; δ<sup>13</sup>C = ˗27.8 ‰) and methane (pMC = 101.6; [CH<sub>4</sub>] = 6460 nM; δ<sup>13</sup>C = ˗71.5 ‰) correspond with modern <sup>14</sup>C ages, suggesting these sources of energy within the habitat are comprised of modern carbon fixed recently by photosynthesizing primary producers at the land surface. By contrast, DOC in the deeper saline groundwater is significantly lower in concentration (21 µM), and substantially older (pMC = 47.3, equates to 6010 ± 95 <sup>14</sup>C yrs). Similarly, dissolved inorganic carbon (DIC) in the freshwater is significantly younger (pMC = 86.5, equates to 1170 ± 15 <sup>14</sup>C yrs) than in the deeper saline water (pMC = 58.4, equates to 4320 ± 25 <sup>14</sup>C yrs). These findings demonstrate that important sources of nutrition for the food web are intimately linked to the overlying subaerial habitat, which suggests these ecosystems are highly vulnerable to nearby land use alterations. Furthermore, this study provides new insights into carbon turnover during the process of methane production/consumption, carbon exchange, and organic matter transformation before the emission of the dissolved constituents into coastal oceans from karst subterranean estuaries. Radiocarbon and stable isotopic analyses of the resident fauna will allow us to evaluate the ecological effects of the rapid top-down transfer mechanism for methane and DOC. Beyond better understanding the sources and fate of these carbon sources, our findings have the potential to support management and conservation efforts aimed at coastal groundwater ecosystems.</p>

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