Heterotrophy in the earliest gut: a single-cell view of heterotrophic carbon and nitrogen assimilation in sponge-microbe symbioses
Laura RixMarta RibesRafel ComaMartin T. JahnJasper M. de GoeijDick van OevelenStéphane EscrigAnders MeibomUte Hentschel
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Abstract:
Sponges are the oldest known extant animal-microbe symbiosis. These ubiquitous benthic animals play an important role in marine ecosystems in the cycling of dissolved organic matter (DOM), the largest source of organic matter on Earth. The conventional view on DOM cycling through microbial processing has been challenged by the interaction between this efficient filter-feeding host and its diverse and abundant microbiome. Here we quantify, for the first time, the role of host cells and microbial symbionts in sponge heterotrophy. We combined stable isotope probing and nanoscale secondary ion mass spectrometry to compare the processing of different sources of DOM (glucose, amino acids, algal-produced) and particulate organic matter (POM) by a high-microbial abundance (HMA) and low-microbial abundance (LMA) sponge with single-cell resolution. Contrary to common notion, we found that both microbial symbionts and host choanocyte (i.e. filter) cells and were active in DOM uptake. Although all DOM sources were assimilated by both sponges, higher microbial biomass in the HMA sponge corresponded to an increased capacity to process a greater variety of dissolved compounds. Nevertheless, in situ feeding data demonstrated that DOM was the primary carbon source for both the LMA and HMA sponge, accounting for ~90% of their heterotrophic diets. Microbes accounted for the majority (65-87%) of DOM assimilated by the HMA sponge (and ~60% of its total heterotrophic diet) but <5% in the LMA sponge. We propose that the evolutionary success of sponges is due to their different strategies to exploit the vast reservoir of DOM in the ocean.Keywords:
Sponge
Microbial food web
Assimilation (phonology)
Nitrogen Cycle
We investigated biomass and composition of the pico-, nano- and microplankton communities in a coastal station of the southeastern Black Sea during 2011. We also examined trophic interactions within these communities from size-fractionated dilution experiments in February, June and December. Autotrophic and heterotrophic biomasses showed similar seasonal trends, with a peak in June, but heterotrophs dominated throughout the year. Autotrophic biomass was mainly comprised by nanoflagellates and diatoms in the first half of the year, and by dinoflagellates and Synechococcus spp. in the second half. Heterotrophic biomass was mostly dominated by heterotrophic bacteria, followed by nanoflagellates and microzooplankton. Dilution experiments suggest that nano- and microzooplankton were significant consumers of autotrophs and heterotrophic bacteria. More than 100% of bacterial production was consumed by grazers in all experiments, while 46%, 21% and 30% of daily primary production were consumed in February, June and December, respectively. In February, autotrophs were the main carbon source, but in December, it was heterotrophic bacteria. An intermediate situation was observed in June, with similar carbon flows from autotrophs and heterotrophic bacteria. Size-fraction dilution experiments suggested that heterotrophic nanoflagellates are an important link between the high heterotrophic bacterial biomass and microzooplankton. In summary, these results indicate that nano- and microzooplankton were responsible for comprising a significant fraction of total microbial plankton biomass, standing stocks, growth and grazing processes. This suggests that in 2011, the microbial food web was an important compartment of the planktonic food web in the coastal southeastern Black Sea.
Microbial food web
Autotroph
Microbial loop
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Prokaryote
Microbial food web
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Growth, grazing, C and nutrient in corporation by the mixotrophic phytoflagellate Poterioochromonas malhamensis were examined under various nutrient and light regimes in the presence of heat‐killed bacteria. Poterioochromonas malhamensis readily ingested bacteria in all culture treatments containing heat‐killed bacteria, and growth rates of the protist were much greater for heterotrophic (bacterivorous) growth than for phototrophic growth. C incorporation efficiencies by the phytoflagellate were virtually identical to P incorporation efficiencies during heterotrophic growth, but N incorporation efficiencies were somewhat lower in nearly all of the treatments. Algal growth in cultures with heat‐killed bacteria was similar in continuous darkness and in continuous light. Bacterial organic C was the primary source of protist cellular C for P. malhamensis during heterotrophic growth. Based on our observations, we conclude that P. malhamensis is primarily heterotrophic and phagotrophic and that it is highly competent in this mode of nutrition.
Mixotroph
Protist
Microbial food web
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Dynamics of autotrophic and heterotrophic prokaryotes and their consumption by nanoflagellates were studied in the euphotic zone at nine stations located from the Levantine Basin (34°E) to the Balearic sea (5°E) in June 1999. Bacterial biomass constituted the largest proportion of living biomass at all stations. Integrated bacterial production at the furthest east station, was sixfold lower than integrated bacterial production at the furthest west (13 and 75 mg C m−2 d−1 respectively). Estimated heterotrophic nanoflagellate bacterivory accounted for 45–87% of bacterial production. Small protists (<3 μm) dominated the bacterivore assemblage and accounted for more than 90% of the heterotrophic bacterial consumption. Our results indicated that there was no negative selection against Synechococcus and that both picoplankton groups were grazed according to their standing stocks. An estimated consumption of Synechococcus derived from food vacuole content analysis of nanoflagellates revealed that they consumed from 0.5 to 45% (mean 13%) of Synechococcus stock per day. These data are among the first documenting the relative grazing impact of heterotrophic nanoflagellates on bacteria and Synechococcus in situ. Assuming that there was no selection for or against Prochlorococcus, heterotrophic nanoflagellates could ingest from 1.4 to 21% (mean 6%) of Prochlorococcus stock per day. The amount of organic carbon obtained by heterotrophic nanoflagellates from photosynthetic prokaryotes represented 27% of the total amount of carbon obtained from total prokaryotes
Picoplankton
Prochlorococcus
Bacterioplankton
Microbial food web
Autotroph
Microbial loop
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