Dataset Information

Impact of Viral Lysis on the Composition of Bacterial Communities and Dissolved Organic Matter in Deep-Sea Sediments.

ABSTRACT: Viral lysis is a main mortality factor for bacteria in deep-sea sediments, leading to changing microbial community structures and the release of cellular components to the environment. Nature and fate of these compounds and the role of viruses for microbial diversity is largely unknown. We investigated the effect of viruses on the composition of bacterial communities and the pool of dissolved organic matter (DOM) by setting up virus-induction experiments using mitomycin C with sediments from the seafloor of the Bering Sea. At the sediment surface, no substantial prophage induction was detected, while incubations from 20 cm below seafloor showed a doubling of the virus-to-cell ratio. Ultra-high resolution mass spectrometry revealed an imprint of cell lysis on the molecular composition of DOM, showing an increase of molecular formulas typical for common biomolecules. More than 50% of these compounds were removed or transformed during incubation. The remaining material potentially contributed to the pool of refractory DOM. Next generation sequencing of the bacterial communities from the induction experiment showed a stable composition over time. In contrast, in the non-treated controls the abundance of dominant taxa (e.g., Gammaproteobacteria) increased at the expense of less abundant phyla. Thus, we conclude that viral lysis was an important driver in sustaining bacterial diversity, consistent with the "killing the winner" model.

SUBMITTER: Heinrichs ME

PROVIDER: S-EPMC7552059 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Impact of Viral Lysis on the Composition of Bacterial Communities and Dissolved Organic Matter in Deep-Sea Sediments.

Heinrichs Mara E ME Tebbe Dennis A DA Wemheuer Bernd B Niggemann Jutta J Engelen Bert B

Viruses 20200822 9

Viral lysis is a main mortality factor for bacteria in deep-sea sediments, leading to changing microbial community structures and the release of cellular components to the environment. Nature and fate of these compounds and the role of viruses for microbial diversity is largely unknown. We investigated the effect of viruses on the composition of bacterial communities and the pool of dissolved organic matter (DOM) by setting up virus-induction experiments using mitomycin C with sediments from the ...[more]

PMID: 32842650

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Project description: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 than 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 lower absorption spectral slope and heterotrophic bacterial growth rate than incubation with Pro-exudate, suggesting that Pro-vDOM was more bioavailable than 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 dominant phytoplankton in the oligotrophic ocean, contributing to the vast majority of marine primary production. Prochlorococcus releases a significant fraction of fixed organic matter into the surrounding environment and supports a vital portion of heterotrophic bacterial activity. Viral lysis is an important biomass loss process of Prochlorococcus However, 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.

Project description:Background:Mono-specific aquaculture effluents contain high concentrations of nutrients and organic matter, which affect negatively the water quality of the recipient ecosystems. A fundamental feature of water quality is its transparency. The fraction of dissolved organic matter that absorbs light is named chromophoric dissolved organic matter (CDOM). A sustainable alternative to mono-specific aquaculture is the multitrophic aquaculture that includes species trophically complementary named "extractive" species that uptake the waste byproducts. Sea cucumbers are recognized as efficient extractive species due to the consumption of particulate organic matter (POM). However, the effects of sea cucumbers on CDOM are still unknown. Methods:During more than one year, we monitored CDOM in two big-volume tanks with different trophic structure. One of the tanks (-holothurian) only contained around 810 individuals of Anemonia sulcata, whereas the other tank (+holothurian) also included 90 individuals of Holothuria tubulosa and Holothuria forskali. We routinely analyzed CDOM absorption spectra and determined quantitative (absorption coefficients at 325 nm) and qualitative (spectral slopes) optical parameters in the inlet waters, within the tanks, and in their corresponding effluents. To confirm the time-series results, we also performed three experiments. Each experiment consisted of two treatments: +holothurians (+H) and -holothurians (-H). We set up three +H tanks with 80 individuals of A. sulcata and 10 individuals of H. tubulosa in each tank and four -H tanks that contained only 80 individuals of A. sulcata. Results:In the time-series, absorption coefficients at 325 nm (a325) and spectral slopes from 275 to 295 nm (S275-295) were significantly lower in the effluent of the +holothurian tank (average: 0.33 m-1 and 16 µm-1, respectively) than in the effluent of the -holothurian tank (average: 0.69 m-1 and 34 µm-1, respectively), the former being similar to those found in the inlet waters (average: 0.32 m-1 and 22 µm-1, respectively). This reduction in the absorption of the dissolved organic matter appears to be mediated by the POM consumption by holothurians. The experiments confirmed the results observed in the time-series. The a325 and S275-295 values were significantly lower in the treatment with holothurians than in the treatment without holothurians indicating a reduction in the concentration of chromophoric organic compounds, particularly of low molecular weight. Discussion:Consequently, sea cucumbers appear to improve water transparency in aquaculture tanks. The underlying mechanism of this improvement might be related to the POM consumption by holothurians, which reduces the concentration of CDOM derived from POM disaggregation or to the direct assimilation of dissolved compounds of low molecular weight as chromophoric amino acids.

Dataset Information

Impact of Viral Lysis on the Composition of Bacterial Communities and Dissolved Organic Matter in Deep-Sea Sediments.

Publications

Impact of Viral Lysis on the Composition of Bacterial Communities and Dissolved Organic Matter in Deep-Sea Sediments.

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