Histophagous ciliate Pseudocollinia brintoni and bacterial assemblage interaction with krill Nyctiphanes simplex. I. Transmission process

Abstract

Histophagous ciliates of the genus Pseudocollinia cause epizootic events that kill adult female krill (Euphausiacea), but their mode of transmission is unknown. We compared 16S rRNA sequences of bacterial strains isolated from stomachs of healthy krill Nyctiphanes simplex specimens with sequences of bacterial isolates and sequences of natural bacterial communities from the hemocoel of N. simplex specimens infected with P. brintoni to determine possible transmission pathways. All P. brintoni endoparasitic life stages and the transmission tomite stage (outside the host) were associated with bacterial assemblages. 16S rRNA sequences from isolated bacterial strains showed that Photobacterium spp. and Pseudoalteromonas spp. were dominant members of the bacterial assemblages during all life phases of P. brintoni and potential pathobionts. They were apparently unaffected by the krill's immune system or the histophagous activity of P. brintoni. However, other bacterial strains were found only in certain P. brintoni life phases, indicating that as the infection progressed, microhabitat conditions and microbial interactions may have become unfavorable for some strains of bacteria. Trophic infection is the most parsimonious explanation for how P. brintoni infects krill. We estimated N. simplex vulnerability to P. brintoni infection during more than three-fourths of their life span, infecting mostly adult females. The ciliates have relatively high prevalence levels (albeit at <10% of sampled stations) and a short life cycle (estimated <7 d). Histophagous ciliate-krill interactions may occur in other krill species, particularly those that form dense swarms and attain high population densities that potentially enhance trophic transmission and allow completion of the Pseudocollinia spp. life cycle.

Histophagous ciliate Pseudocollinia brintoni and bacterial assemblage interaction with krill Nyctiphanes simplex. II. Host responses

“…Because we observed that concentrations of bacteria in the stomach and hemocoel decreased during the early stages of infection, we propose that a ROS burst occurred to counteract the initial inflow of bacteria entering with the ciliates through the tro phic transmission pathway (Gómez-Gutiérrez et al 2015). The ROS burst may be effective to eliminate most of the bacteria because we observed changes in bacterial assemblages over time, but insufficient to stop histophagous ciliate P. brintoni infection and several pathobiont bacterial strains observed in all studied P. brintoni infection phases (Photobacterium spp.…”

“…and Pseudoalteromonas spp. ; Gómez-Gutiérrez et al 2015). Inhibition of SOD and GR activities from the first stage of infection suggests that hydrogen peroxide was present in considerable amounts and that ROS was neutralized by CAT and Se-GPx.…”

“…does) (Bradbury & Goyal 1976, Johnson & Bradbury 1976, Bradbury 1994, and infection by krill mating . The trophic infection mechanism was indirectly evidenced by comparing bacterial communities inhabiting the sto machs of healthy krill and those detected in the hemocoel of specimens infected with P. brintoni (Gómez-Gutiérrez et al 2015). However, little is known about the immune system response and physio logical changes of krill (Zhao et al 2011, Seear et al 2012, resulting in a poor and fragmented understanding about the effect of pathogens and para sites on euphausiids.…”

Review paper Pseudocollinia histophagous ciliates infect krill in the Pacific and Atlantic Oceans and possibly worldwide

“…Firstly, two species of dinoflagellates (Chytriodinium roseum and C. affine) that kill eggs of Meganyctiphanes norvegica (M Sars, 1857) in the Mediterranean Sea (Dogiel, 1906;Cachon & Cachon, 1968;Daugbjerg et al, 2000; and eggs of Euphausia pacifica Hansen, 1911 off the Oregon coasts (USA) (Gómez-Gutiérrez et al, 2009). Secondly, apostome ciliates of the genus Pseudocollinia, discovered 80 years later (Capriulo & Small, 1986;Capriulo et al, 1991;Gómez-Gutiérrez et al, 2003, 2015aLynn et al, 2014). Apostome histophagous ciliates can cause massive die-offs of krill because they have short life cycles, relatively high transmission rates, and capacity to transform host biomass into reproduc-review paper tive and transmission cells that kill the crustacean host (Gómez-Gutiérrez et al, 2003, 2012, 2015aChantangsi et al, 2013;Lynn et al, 2014).…”

“…Secondly, apostome ciliates of the genus Pseudocollinia, discovered 80 years later (Capriulo & Small, 1986;Capriulo et al, 1991;Gómez-Gutiérrez et al, 2003, 2015aLynn et al, 2014). Apostome histophagous ciliates can cause massive die-offs of krill because they have short life cycles, relatively high transmission rates, and capacity to transform host biomass into reproduc-review paper tive and transmission cells that kill the crustacean host (Gómez-Gutiérrez et al, 2003, 2012, 2015aChantangsi et al, 2013;Lynn et al, 2014). The genus Pseudocollinia currently includes four extant species: P. beringensis (Capriulo & Small, 1986), P. oregonensis (Gómez-Gutiérrez et al, 2006), P. brintoni Gómez-Gutiérrez et al, 2012, andP.…”