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Deciphering associations between dissolved organic molecules and bacterial communities in a pelagic marine system.

ABSTRACT: Dissolved organic matter (DOM) is the main substrate and energy source for heterotrophic bacterioplankton. To understand the interactions between DOM and the bacterial community (BC), it is important to identify the key factors on both sides in detail, chemically distinct moieties in DOM and the various bacterial taxa. Next-generation sequencing facilitates the classification of millions of reads of environmental DNA and RNA amplicons and ultrahigh-resolution mass spectrometry yields up to 10?000 DOM molecular formulae in a marine water sample. Linking this detailed biological and chemical information is a crucial first step toward a mechanistic understanding of the role of microorganisms in the marine carbon cycle. In this study, we interpreted the complex microbiological and molecular information via a novel combination of multivariate statistics. We were able to reveal distinct relationships between the key factors of organic matter cycling along a latitudinal transect across the North Sea. Total BC and DOM composition were mainly driven by mixing of distinct water masses and presumably retain their respective terrigenous imprint on similar timescales on their way through the North Sea. The active microbial community, however, was rather influenced by local events and correlated with specific DOM molecular formulae indicative of compounds that are easily degradable. These trends were most pronounced on the highest resolved level, that is, operationally defined 'species', reflecting the functional diversity of microorganisms at high taxonomic resolution.

SUBMITTER: Osterholz H

PROVIDER: S-EPMC4918438 | biostudies-literature | 2016 Jul

REPOSITORIES: biostudies-literature

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Deciphering associations between dissolved organic molecules and bacterial communities in a pelagic marine system.

Osterholz Helena H Singer Gabriel G Wemheuer Bernd B Daniel Rolf R Simon Meinhard M Niggemann Jutta J Dittmar Thorsten T

The ISME journal 20160122 7

Dissolved organic matter (DOM) is the main substrate and energy source for heterotrophic bacterioplankton. To understand the interactions between DOM and the bacterial community (BC), it is important to identify the key factors on both sides in detail, chemically distinct moieties in DOM and the various bacterial taxa. Next-generation sequencing facilitates the classification of millions of reads of environmental DNA and RNA amplicons and ultrahigh-resolution mass spectrometry yields up to 10 00 ...[more]

PMID: 26800236

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Project description:Marine dissolved organic matter (DOM) is a complex mixture of chemical compounds. At 750 Pg C, it is one of the biggest pools of reduced carbon on Earth. It has been proposed that the diversity of DOM is responsible for its recalcitrance. We hypothesize that the chemodiversity of marine DOM is a reflection of the chemodiversity of bacterial exometabolomes. To test this, we incubated two model strains of the Roseobacter group; Phaeobacter inhibens and Dinoroseobacter shibae in pure culture using three different simple organic compounds as sole carbon sources (glutamate, glucose, and acetate and succinate for P. inhibens and D. shibae, respectively). The exometabolome of the model organisms was characterized using Fourier Transform Ion Cyclotron Resonance Mass Spectrometry (FT-ICR-MS) and ecological diversity measures. We detected thousands of molecular masses in the exometabolomes of P. inhibens and D. shibae (21,105 and 9,386, respectively), reflecting the capability of single bacterial strains to diversify simple organic compounds. The chemical composition of the exometabolomes changed with growth phase and also differed according to the strain incubated and the utilized substrate. We mimicked a higher diversity of substrates, bacterial species and heterogeneous growth (different growth phases) to approach the complexity of natural environments, by computationally creating combinations of detected exometabolomes. We compared the chemodiversity of these combinations, indicative for chemodiversity of freshly produced microbial DOM to that of refractory DOM from one of the oldest oceanic water masses (North Equatorial Pacific Intermediate Water). Some combinations of exometabolomes showed higher richness than the deep ocean refractory DOM, and all the combinations showed higher functional diversity. About 15% of the 13,509 molecular formulae detected in exometabolomes and refractory oceanic DOM were shared, i.e., occurred in Roseobacter exometabolomes and in deep water samples. This overlap provides further support for our hypothesis that marine bacteria from the Roseobacter group contribute to the sustainability of marine DOM chemodiversity and stability.

Project description:The Amazon River basin sustains dramatic hydrochemical gradients defined by three water types: white, clear, and black waters. In black water, important loads of allochthonous humic dissolved organic matter (DOM) result from the bacterioplankton degradation of plant lignin. However, the bacterial taxa involved in this process remain unknown, since Amazonian bacterioplankton has been poorly studied. Its characterization could lead to a better understanding of the carbon cycle in one of the Earth's most productive hydrological systems. Our study characterized the taxonomic structure and functions of Amazonian bacterioplankton to better understand the interplay between this community and humic DOM. We conducted a field sampling campaign comprising 15 sites distributed across the three main Amazonian water types (representing a gradient of humic DOM), and a 16S rRNA metabarcoding analysis based on bacterioplankton DNA and RNA extracts. Bacterioplankton functions were inferred using 16S rRNA data in combination with a tailored functional database from 90 Amazonian basin shotgun metagenomes from the literature. We discovered that the relative abundances of fluorescent DOM fractions (humic-, fulvic-, and protein-like) were major drivers of bacterioplankton structure. We identified 36 genera for which the relative abundance was significantly correlated with humic DOM. The strongest correlations were found in the Polynucleobacter, Methylobacterium, and Acinetobacter genera, three low abundant but omnipresent taxa that possessed several genes involved in the main steps of the β-aryl ether enzymatic degradation pathway of diaryl humic DOM residues. Overall, this study identified key taxa with DOM degradation genomic potential, the involvement of which in allochthonous Amazonian carbon transformation and sequestration merits further investigation. IMPORTANCE The Amazon basin discharge carries an important load of terrestrially derived dissolved organic matter (DOM) to the ocean. The bacterioplankton from this basin potentially plays important roles in transforming this allochthonous carbon, which has consequences on marine primary productivity and global carbon sequestration. However, the structure and function of Amazonian bacterioplanktonic communities remain poorly studied, and their interactions with DOM are unresolved. In this study, we (i) sampled bacterioplankton in all the main Amazon tributaries, (ii) combined information from the taxonomic structure and functional repertory of Amazonian bacterioplankton communities to understand their dynamics, (iii) identified the main physicochemical parameters shaping bacterioplanktonic communities among a set of >30 measured environmental parameters, and (iv) characterized how bacterioplankton structure varies according to the relative abundance of humic compounds, a by-product from the bacterial degradation process of allochthonous DOM.

Dataset Information

Deciphering associations between dissolved organic molecules and bacterial communities in a pelagic marine system.

Publications

Deciphering associations between dissolved organic molecules and bacterial communities in a pelagic marine system.

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