Copepod guts as biogeochemical hotspots in the sea: Evidence from microelectrode profiling of Calanus spp

Abstract

The environmental conditions inside the gut of Calanus hyperboreus and C. glacialis were measured with microelectrodes. An acidic potential hydrogen (pH) gradient was present in the gut of C. hyperboreus, and the lowest pH recorded was 5.40. The gut pH of a starved copepod decreased by 0.53 after the copepod resumed feeding for a few hours, indicating the secretion of acidic digestive fluid. A copepod feeding on Thalassiosira weissflogii (diatom) had slightly lower pH than that feeding on Rhodomonas salina (cryptophyte). Oxygen was undersaturated in the gut of both C. hyperboreus and C. glacialis, with a steep gradient from the anal opening to the metasome region. The central metasome region was completely anoxic. Food remains in the gut led to a lower oxygen level, and a diatom diet induced a stronger oxygen gradient than a cryptophyte diet. The acidic and suboxic-anoxic environments of the copepod gut may support iron dissolution and anaerobic microbial activities that otherwise are not favored in the well-buffered and oxygenated ambient ocean.

The microbiome of North Sea copepods

“…Although we observed several phylotypes related to Sulfitobacter which were previously described for fresh faecal pellets (Jing et al 2012), the assignment of specific bacterial populations to different body compartments of copepods remains highly speculative. Since the copepod's gut displays environmental conditions which are fundamentally different from those of the surrounding seawater (Tang et al 2011), it can be assumed that growth of specific bacterial populations is favoured there. Unfortunately, detailed histological studies of copepods with a focus on bacteria colonising the intestine of copepods are still extremely rare (Peter and Sommaruga 2008).…”

The regeneration of highly bioavailable iron by meso‐ and microzooplankton

“…Copepod guts and protist digestive vacuoles differ in pH and oxygen saturation. The overall gut pH of copepods appears to be less acidic than the digestive vacuoles of protists (Fok et al 1982;Pond et al 1995;Tang et al 2011). Although a pH as low as 3, as observed during the fusion of digestive vacuoles with lysosomes, could contribute potentially to the stabilization and release cellular ferrous Fe, the subsequent pH rise to 7 during the active digestion stage, which is characterized by the release of digestive enzymes (Fok et al 1982), makes the egestion of Fe(II) less likely.…”

“…Additionally, the ingestion of different prey also affects the degree of oxygen saturation within different parts of the copepod gut. Feeding a copepod with the diatom T. weissflogii did not only decrease the pH, but also led to a stronger oxygen gradient than feeding with a cryptophyte (Tang et al 2011). The combination of lower pH and extended oxygen undersaturation inside the gut, and also a short gut passage time when feeding on a diatom prey (Besiktepe and Dam 2002), may cause copepod grazers to release more digestive fluid of a lower pH, resulting in a higher Fe(II) : Fe(III) ratio, potentially increasing the residence time of egested ferrous Fe into the surrounding seawater.…”

“…However, different proteinase classes detected in the copepod Calanus finmarchicus can show significant pH affinities, whereby metallo-and serine-proteinases are dominant at neutral or alkaline pH, and aspartic proteinases are dominant under acidic conditions (Solgaard et al 2007). Additionally, some copepod gut regions are characterized by low oxygen saturation during digestion, which is also affected by the chemical composition of the prey (Tang et al 2011). Consequently, the existence of different chemical and biological conditions in grazers may lead to the degradation of different proteins and subsequently to differences in the bioavailability of the regenerated Fe.…”

“…Subsequently, the pH in the digestive vacuoles rises from 3 to 7, accompanied by acid phosphotase activity, which suggests active digestion (Fok et al 1982). In contrast to the temporal pH changes inside digestive vacuoles, pH in the gut of copepods varies spatially between 5.4 and 9.35 and can vary with the chemical composition of the ingested prey (Pond et al 1995;Tang et al 2011). pH appears to have only a minor effect on the specific proteinase activity, with the highest activity at ca.…”