Does the Chemodiversity of Bacterial Exometabolomes Sustain the Chemodiversity of Marine Dissolved Organic Matter?

Beatriz E Noriega-Ortega,Andrea Mentges,Thorsten Dittmar,Meinhard Simon,Gerrit Wienhausen,Jutta Niggemann

doi:10.3389/fmicb.2019.00215

Abstract

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.

Highlights

Marine dissolved organic matter (DOM) is one of the most complex molecular mixtures on our planet
The results reported here are based on the same data as the study presented by Wienhausen et al (2017), who report the detection of specific precursors of vitamins, amino acids, growth factors and quorum sensing molecules in the exometabolome, suggesting that the investigated strains act as helpers for other marine microbes by providing biosynthetic precursors and other molecules as public goods
Pure cultures of P. inhibens and D. shibae were sampled at different growth stages determined by optical density (Figure 1A)

Summary

Introduction

Marine dissolved organic matter (DOM) is one of the most complex molecular mixtures on our planet. Thousands (>10,000) of compounds have been identified within this mixture (Riedel and Dittmar, 2014). DOM is operationally classified into reactivity fractions ranging from labile to ultra-refractory (Hansell, 2013). The refractory fraction, in contrast, accumulates in the ocean for decades to millennia (Williams et al, 1969; Bauer et al, 1992; Hansell, 2013) and comprises 70 – 95% of total DOM (Hedges et al, 2000; Ogawa et al, 2001). The reasons for the long-term stability of DOM in the oceans are still discussed (Dittmar, 2015). The “dilution hypothesis” proposes that given the extremely high chemodiversity of DOM, the concentrations of single compounds are very low limiting the encounter rate of microbes to identical molecules and preventing microbial degradation (Barber, 1968; Arrieta et al, 2015)

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Conclusion