A Crispy Diet: Grazers of Achromatium oxaliferum in Lake Stechlin Sediments
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Achromatium is the largest freshwater bacterium known to date and easily recognised by conspicuous calcite bodies filling the cell volume. Members of this genus are highly abundant in diverse aquatic sediments and may account for up to 90% of the bacterial biovolume in the oxic-anoxic interfaces. The high abundance implies that Achromatium is either rapidly growing or hardly prone to predation. As Achromatium is still uncultivated and does not appear to grow fast, one could assume that the cells might escape predation by their unusual shape and composition. However, we observed various members of the meiofauna grazing or parasitizing on Achromatium. By microphotography, we documented amoebae, ciliates, oligochetes and plathelminthes having Achromatium cells ingested. Some Achromatium cells harboured structures resembling sporangia of parasitic fungi (chytrids) that could be stained with the chitin-specific dye Calcofluor White. Many Achromatia carried prokaryotic epibionts in the slime layer surrounding the cells. Their regular distribution over the cell might indicate that they are commensalistic rather than harming their hosts. In conclusion, we report on various interactions of Achromatium with the sediment community and show that although Achromatium cells are a crispy diet, full of calcite bodies, predators do not spare them.
KeywordsLarge sulfur bacteria Plathelminthes Ciliates Amoebae Oligochetes Aquatic fungi
Achromatium is the genus with the largest freshwater bacteria known to date. Single cells with a length of up to 125 μm  are visible even with the naked eye. The volume of an Achromatium cell exceeds that of a “normal” bacterium by a factor of 104–105 . Like other large sulfur-oxidising bacteria, such as Beggiatoa and Thiomargarita [3, 4], Achromatium cells contain small sulfur globules. In a recent study, we have shown that single Achromatium cells harbour multiple DNA spots showing a community-like genome diversity . Phenotypically most conspicuous and unique to Achromatium are numerous intracellular calcite bodies (CaCO3), which fill major parts of the cell volume . The biological role of these calcite bodies is under debate [7, 8].
Achromatium can be found within the oxic-anoxic transition zone in freshwater [2, 6, 9, 10, 11, 12], brackish , and marine  sediments and may reach cell counts of 103–105 cells per cubic centimetre accounting for 90% of the bacterial biovolume in these layers [6, 14, 15]. The high abundance of Achromatium implies that the cells are either rapidly growing or not prone to predation. As Achromatium is uncultivated exact growth rates are unknown. Mortality factors, such as predation and parasitism, which might reduce natural population sizes of Achromatium, have neither been reported. However, for grazers Achromatium cells might be unattractive as food source due to the massive amounts of calcite. Thus, we assumed that the cells might escape predation by their unusual size and composition.
During a series of physiological experiments Achromatium cells were collected from sediment storages in glass jars and microscopically examined. In doing so, we repeatedly detected grazers that contained ingested Achromatium cells and took microphotographs of them. We present here a qualitative description that sheds new light on the ecological relationships of Achromatium with the sediment community.
To estimate the natural abundance of the grazers in the sediment of Lake Stechlin, we took cores of fresh sediment. The cores were subsequently divided into oxic surface layer (0–3 mm), oxic-anoxic transition zone (6–10 mm) and anoxic layer (10–15 mm). The sediment samples were filtered through an 80-μm mesh to wash out small organisms (e.g. ciliates), the unsieved sediment was analysed for the presence of larger grazers.
Epifluorescence microscopy (Olympus BX51) and Sybr Green I were used to visualize mucous-associated prokaryotes. To study fungal infections, Achromatium cells were stained with Calcofluor White, a fluorescent dye used to stain fungal chitin. Pictures were taken with a Canon EOS 600D camera from live samples and further processed with PICOLAY .
Grazers Ingesting Achromatium Cells
Many Achromatium cells were covered by slime, harbouring prokaryotic epibionts [6, 14], as shown by epifluorescence microscopy with Sybr Green I. Sometimes, a uniform morphotype, either rod-shaped or coccoid cells (Fig. 3a) was dominating on single Achromatium cells. The associated bacteria were evenly distributed within the slime matrix indicating a beneficial or commensalistic relation. The formation of micro-colonies, as indication for rapid proliferation during substrate degradation was not observed.
Our observations show that Achromatium is exposed to selective pressure through predation and parasitism. Living at the shallow sediment-water interface, or slightly below, Achromatium is easily accessible for grazers that are adapted to the interstitial habitat. Although the cells are unusually large and full of calcite bodies, there are a variety of organisms grazing on them. Typically, food vacuoles have a low pH. The calcite present in ingested Achromatium cells might buffer this, and digestion will require additional acidification . Thus, acidic digestion compartments can help to overcome the challenges when feeding on such “crispy” bacteria. Whereas calcite has no nutritional value, other cellular components of Achromatium such as the surrounding mucous matrix and the epibionts might represent an attractive food source for grazers. Although our samples, derived from fresh sediment as well as from stored sediment of varying ages, were not suited for a quantitative analysis, we assume that grazers from several groups control the population density of Achromatium in its natural habitat. The observed grazers resembled common organisms of freshwater environments [18, 19]. As these grazers do not seem to be specialised to feed on Achromatium a similar grazing pressure might affect also brackish and marine populations. Fungal infection might be an additional mortality factor for natural populations. It was previously shown that cyanobacteria are infected by parasitizing chytrids . Given their widespread abundance in freshwater and marine environments it is likely that also Achromatium is a host for them.
Therefore, our initial hypothesis that Achromatium is not prone to predation has to be rejected. Instead, they are exposed to considerable pressure from parasites and grazers and have to compensate this with a corresponding growth rate.
We thank Hans-Peter Grossart, Silke Van den Wyngaert and Hans-Dietrich Babenzien (Leibniz Institute of Freshwater Ecology and Inland Fisheries, Stechlin, Germany), Verena Carvalho (Max Planck Institute for Marine Microbiology, Bremen, Germany), and Bert Engelen (ICBM) for valuable discussions and helpful comments on the manuscript. Furthermore, we thank Wilko Ahlrichs (University of Oldenburg) for the help with the classification of the grazers.
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Conflict of Interest
The authors declare that they have no conflict of interest.
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