Identifying and quantifying nitrogen pools is essential for understanding the nitrogen cycle in aquatic ecosystems. The ubiquitous diatoms represent an overlooked nitrate pool as they can accumulate nitrate intracellularly and utilize it for nitrogen assimilation, dissipation of excess photosynthetic energy, and Dissimilatory Nitrate Reduction to Ammonium (DNRA). Here, we document the global co-occurrence of diatoms and intracellular nitrate in phototrophic microbial communities in freshwater (n = 69), coastal (n = 44), and open marine (n = 4) habitats. Diatom abundance and total intracellular nitrate contents in water columns, sediments, microbial mats, and epilithic biofilms were highly significantly correlated. In contrast, diatom community composition had only a marginal influence on total intracellular nitrate contents. Nitrate concentrations inside diatom cells exceeded ambient nitrate concentrations ∼100–4000-fold. The collective intracellular nitrate pool of the diatom community accounted for <1% of total nitrate in pelagic habitats and 65–95% in benthic habitats. Accordingly, nitrate-storing diatoms are emerging as significant contributors to benthic nitrogen cycling, in particular through Dissimilatory Nitrate Reduction to Ammonium activity under anoxic conditions.
Copepod carcasses are prevalent in marine ecosystems and might represent an important component of the sinking flux of particulate organic carbon in the ocean. The extent to which copepod carcasses contribute to the biological carbon pump is controlled by different environmental factors, including temperature. However, the effect of temperature on the longer-term kinetics of carbon mineralization of copepod carcasses is not well-studied. We conducted laboratory experiments to quantify the carbon mineralization associated with sinking carcasses of the cosmopolitan copepod Acartia tonsa through aerobic microbial respiration at 5 temperatures (20, 16, 12, 8, and 4°C). Microbial respiration rates associated with the carcasses were positively correlated with temperature and characterized by an initial short lag-phase, a rapid increase to a maximum rate, and a subsequent gradual decline in the rate of degradation. On average, 50% of the total carbon of the carcasses was mineralized within 6-12 d at 20°C, versus >60 d at 4°C. During the incubations, most carbon mineralization occurred in the ambient seawater, likely fueled by dissolved organic carbon leaking from the carcasses into the surrounding seawater. Extrapolating measured carbon turnover and sinking rates suggests that at 20°C, the mineralization of sinking copepod carcasses is constrained to the surface ocean. In contrast, at 4°C, sinking copepod carcasses can reach the deep ocean before they have been completely degraded. Hence, in low-temperature regions, copepod carcasses may represent an important agent for carbon export through the biological carbon pump.
Krill represent a major link between primary producers and higher trophic levels in polar marine food webs. Potential links to lower trophic levels, such as heterotrophic microorganisms, are less well documented. Here, we studied the kinetics of microbial degradation of sinking carcasses of two dominant krill species Thysanoessa raschii and Meganyctiphanes norvegica from Southwest Greenland. Degradation experiments under oxic conditions showed that 6.0-9.1% of carbon and 6.4-7.1% of nitrogen were lost from the carcasses after one week. Aerobic microbial respiration and the release of dissolved organic carbon were the main pathways of carbon loss from the carcasses. Ammonium release generally contributed the most to carcass nitrogen loss. Oxygen micro profiling revealed anoxic conditions inside krill carcasses/specimens, allowing anaerobic nitrogen cycling through denitrification and dissimilatory nitrate reduction to ammonium (DNRA). Denitrification rates were up to 5.3 and 127.7 nmol N carcass-1 d-1 for T. raschii and M. norvegica, respectively, making krill carcasses hotspots of nitrogen loss in the oxygenated water column of the fjord. Carcass-associated DNRA rates were up to 4-fold higher than denitrification rates, but the combined activity of these two anaerobic respiration processes did not contribute significantly to carbon loss from the carcasses. Living krill specimens did not harbor any significant denitrification and DNRA activity despite having an anoxic gut as revealed by micro profiling. The investigated krill carcasses sink fast (1500-3000 m d-1) and our data show that only a small fraction of the associated carbon is lost during descent. Based on data on krill distribution, our findings are used to discuss the potential importance of sinking krill carcasses for sustaining benthic food webs in the Arctic.
Euphausiids (krill) are important contributors to marine biomass and key players in marine pelagic trophic webs. Euphausiid stomachs represent a specific niche for microbes that participate in the digestion of the host’s dietary components. Methods for the study of the diversity and function of these microorganisms remain complex. Bacterial ribosomal sequences obtained from lysates of stomachs are often overrepresented by organisms from the surrounding environment. Flow cytometry with cell sorting (FC-CS) have become a powerful technique to study microbial community structure but also for the study of population genomics of gut-associated bacteria. We compared the performance of the FC-CS-sequencing and total DNA extraction-sequencing to study the stomach microbiota of the Humboldt Current krill. Non-specific amplification was not retrieved in the polymerase chain reaction (PCR) from cells sorted, opposite to the observed using the DNA from the whole lysate. Sequences obtained from the whole stomach DNA were enriched in picocyanobacteria, whereas sequences retrieved from cells sorted belonged almost exclusively to Balneola sp. of the new phylum Balneolaeota. Our results suggest that the stomach-associated microbiota can be successfully characterized by FC-CS and sequencing by manual scraping of the stomach. The implementation of this technique might complement future studies on host-microbes interaction and their implications on the marine pelagic food web.
Euphausiids (or krill) are important contributors to marine biomass and key players in marine pelagic trophic webs. Euphausiids stomachs represent a specific niche for microbes that participate in the digestion of the host dietary components. To date, methods for the study of the diversity and function of these microorganisms remain complex. Often, bacterial ribosomal sequences obtained from lysates of stomachs are overrepresented by organisms from the surrounding environment. Flow cytometry with cell sorting (FC-CS) have become a powerful technique to study microbial community structure but also for the study of population genomics of gut-associated bacteria, even at a single-cell level.In this study, we used FC-CS and sequencing of the bacterial 16S rRNA gene to study the microorganisms inhabiting the stomach of the Humboldt Current krill, Euphausia mucronata. This approach was complemented with DNA extraction and sequencing from whole lysate stomachs as described for other crustacean species.Non-specific amplification was not retrieved in the polymerase chain reaction (PCR) from cells sorted, opposite to the observed using the DNA from the whole lysate. Sequences obtained from the whole stomach DNA were enriched in picocyanobacteria, meanwhile, sequences retrieved from cells sorted belonged almost exclusively to Balneola sp. of the new phylum, Balneolaeota. This study represents, to our knowledge, the first report of Balneola sp. in the stomach for any organism inhabiting the Humboldt Current System (HCS).Our results suggest that the stomach-associated microbiota can be characterized by FC-CS and sequencing by manual scraping of the stomach coupled with the DNA extraction and sequencing. This work represents a baseline for similar studies of other mesozooplankton groups. The implementation of this technique might complement future studies on host-microbes’ interaction and their implications on the marine pelagic food web.
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