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Katrin Knittel

David Probandt

In the oceans, about 20% of primary production takes place at continental shelves (Jahnke, 2010), making them a hot spot for global carbon cycling. 

The first interaction of water column-derived organic matter with benthic microbial communities takes place in surface sediments which are acting as biological filters catalyzing central steps of elemental cycling.


Sampling of sediment cores
Sampling of sediment cores
Sand grains
A view through a binocular: Sand grains. © MPI-MM

Life on a sand grain

Marine sediments constitute the natural habitat for estimated
5.39 x 1029 bacteria and archaea (Parkes et al., 2014). In surface sediments, cell abundances are 108 to 109 per gram, and even for the subsurface seabed, more than 105 cells per gram have been reported.

More than 99% of the benthic microbial community lives attached to sand grains (Rusch et al., 2003). Thus, cell numbers per sand grain vary between 40,000 and one million depending on size or surface characteristics of the grains or other factors. Resuspension of sediment grains exposes the microbial community to mechanical shearing stress and constantly changing environmental conditions. Based on 16S rRNA gene sequencing of environmental DNA extracted from several grams of sediment, North Sea surface sediments were found to accommodate up to 12,000 bacterial species (Probandt et al., 2017).

In this project we go beyond bulk sediment analysis by taking a direct look at single sand grains to study the microbes in their natural habitat (Probandt & Knittel, unpublished). Adapted protocols for hybridization or PCR of single sand grains without prior sonication or DNA extraction allows us to study the microbial community composition and structure in situ.

Microbes on a sand grain
Microbes on a sand grain (stained with SYBR green).
© D. Probandt, MPI-MM.

Already the first 5 mm of the sediments are populated by microbial communities remarkably different from those in bottom waters. In particular, the much lower abundances of alphaproteobacterial SAR11, gammaproteobacterial SAR86 and “Candidatus Actinomarina” (clade OM1) in surface sediments indicate a minor relevance of these groups in the benthos and indicate that other groups are responsible for element cycling.

Sediment permeability has a clear influence on community composition. For example, Desulfobacteraceae and Flavobacteriaceae are more abundant in impermeable than in highly permeable sediments where acidobacterial Sva0725 dominate. In comparison, myxobacterial Sandaracinaceae are most abundant in medium permeable sediments while Woeseiaceae/JTB255 and Planctomycetes are major groups in all surface sediment types (Probandt et al., 2017).

Unlike planktonic flavobacteria, cultivated benthic species have no or only limited capabilities to degrade macromolecules. They rather use simple carbohydrates or are fermentative bacteria. Fermentation products, such as ethanol and fatty acids, might be used by myxobacterial Sandaracinaceae. Periods of anoxia regularly occur in highly dynamic permeable surface sediments. In the absence of oxygen, remineralization of organic matter is mediated through dissimilatory sulfate reduction by Desulfobacteraceae and Desulfobulbaceae. Biogenically formed reduced sulfur species feed sulfide-oxidizing autotrophic Acidiferrobacter and Sulfurovum/Sulfurimonas. Members of the Woeseiaceae/JTB255 (Dyksma et al., 2016; Mussmann et al., 2017) are metabolically diverse and likely also involved in sulfide oxidation.

Microbial degradation of organic matter in surface sediments
Particulate and dissolved organic matter is transported into the sediment where it is remineralized by heterotrophic microbial communities. Physical mixing of top sediment layers occurs by advective sediment transport. Light brown shaded area schematically indicates the zone of fluctuating redox conditions. Different colour of benthic and planktonic Flavobacteriia indicates different species composition.
Abbreviations: Phyc, Phycisphaerae; Plancto, Planctomycetia; Flavo, Flavobacteriaceae; Acido, acidobacterial subgroup22 and clade Sva0725; D’bacteraceae, Desulfobacteraceae.
© D. Probandt, MPI-MM

Sulfur bacteria

Marc Mußmann et al.

A long term goal is to uncover the ecology and ecophysiology of key sulfur-oxidizing bacteria in marine sediments. For this purpose, we study large sulfur bacteria (LSB) of the family Beggiatoaceae. A partial genome of "Candidatus Thiomargarita nelsonii" that was derived from a single cell (Winkel et al., 2016) revealed a high metabolic flexibility such as different energy-yielding pathways including nitrate respiration and hydrogen oxidation. "Ca. T. nelsonii" and close relatives are the first free-living microbes shown to encode two carbon-fixation pathways, namely the CBB- and the rTCA pathways.

Conspicuous sulfur oxidizers such as LSB and cable bacteria reach high abundances only at relatively few sites of the seafloor. Therefore we searched for sulfur oxidizers that are possibly ubiquitously abundant in marine (coastal) sediments. We have detected high relative cell and sequence abundances of the families Woeseiaceae/JTB255, Acidiferrobacteraceae and other Gammaproteobacteria in sediments worldwide (Lenk et al. 2011, Dyksma et al., 2016).

Collectively, the identified sulfur oxidizers may amount to average cell abundances of impressive ~100 million cells cm-3 in diverse organic-rich marine sediments, equaling approximately 10% of total microbial cell counts in these habitats.

Single cell and metagenomic analysis combined with isotopic tracer experiments indicated a broad physiological range of Woeseiaceae/JTB255 including heterotrophy and a facultative sulfur- or hydrogen-dependent autotrophy. The broad range of energy-yielding metabolisms possibly explains the ubiquity and high abundance of Woeseiaceae/JTB255 in marine sediments (Mußmann et al., 2017). Together with Acidiferrobacteraceae and relatives of Oligobrachia tubeworm symbionts (SSr-group), Woeseiaceae, accounted for >70% of microbial dark CO2 fixation in sediments along the European Atlantic coastline (Dyksma et al., 2016).

Global distribution of Woeseiaceae
Global distribution and abundance of Woeseiaceae/JTB255 in marine surface sediments. Woeseiaceae/JTB255 are ubiquitous and consistently rank among the most abundant 16S rRNA gene sequences retrieved from diverse marine sediments. They accounted for up to 22% of bacterial amplicons and 6% of total cell counts in European and Australian coastal sediments.
Red dots: Woeseiaceae were the most abundant group of all bacterial groups.
Yellow dots: Woeseiaceae were among top ten most abundant groups.
Blue dots: Woeseiaceae detected but no quantitative data available.
Triangles: Woeseiaceae made up 2-6% of total cell counts.
Figure adapted from Mußmann et al. 2017.
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