Abstract
Experiments with bacteria in culture have shown that they often display “feast and famine” strategies that allow them to respond with fast growth upon pulses in resource availability, and enter a growth-arrest state when resources are limiting. Although feast responses have been observed in natural communities upon enrichment, it is unknown whether this blooming ability is maintained after long periods of starvation, particularly in systems that are energy limited like the bathypelagic ocean. Here we combined bulk and single-cell activity measurements with 16S rRNA gene amplicon sequencing to explore the response of a bathypelagic community, that had been starved for 1.6 years, to a sudden organic carbon supply. We observed a dramatic change in activity within 30 h, with leucine incorporation rates increasing over two orders of magnitude and the number of translationally active cells (mostly Gammaproteobacteria) increasing 4-fold. The feast response was driven by a single operational taxonomic unit (OTU) affiliated with the Marinobacter genus, which had remained rare during 7 months of starvation. Our work suggests that bathypelagic communities harbor a seed bank of highly persistent and resourceful “feast and famine” strategists that might disproportionally contribute to carbon fluxes through fast responses to occasional pulses of organic matter.
Highlights
The bathypelagic realm, the layer of the ocean between 1000 and 4000 m depth, is one of the largest habitats on Earth, and contains three-quarters of the pelagic marine prokaryotic biomass (Arístegui et al, 2009)
Organic carbon was supplied by mixing 4 parts of bathypelagic water with 1 part of 0.2 μm-filtered freshly collected surface seawater, which represented an increase in the dissolved organic carbon concentration (DOC) of 9 μM over the ∼44 μM that had remained constant during the 1.6 years (Figures 1A,B)
Conditions that allow sustained growth are rare in nature, and some heterotrophic bacteria adapt to this situation by alternating periods of growth with non-growth (Kjelleberg et al, 1993)
Summary
The bathypelagic realm, the layer of the ocean between 1000 and 4000 m depth, is one of the largest habitats on Earth, and contains three-quarters of the pelagic marine prokaryotic biomass (Arístegui et al, 2009). Given the sporadic nature of the carbon supply, deep ocean heterotrophic prokaryotes should be able of persisting as inactive or dormant (i.e., in an state of low metabolic activity (Kjelleberg et al, 1993) for long times, and when inactive, such taxa would comprise a bathypelagic microbial seed bank (sensu Lennon and Jones, 2011) that may ensure a quick response of communities to any sudden resource input.
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