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Front Immunol
2020 Jan 01;11:608066. doi: 10.3389/fimmu.2020.608066.
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Ecological Factors Mediate Immunity and Parasitic Co-Infection in Sea Fan Octocorals.
Tracy AM
,
Weil E
,
Burge CA
.
Abstract
The interplay among environment, demography, and host-parasite interactions is a challenging frontier. In the ocean, fundamental changes are occurring due to anthropogenic pressures, including increased disease outbreaks on coral reefs. These outbreaks include multiple parasites, calling into question how host immunity functions in this complex milieu. Our work investigates the interplay of factors influencing co-infection in the Caribbean sea fan octocoral, Gorgonia ventalina, using metrics of the innate immune response: cellular immunity and expression of candidate immune genes. We used existing copepod infections and live pathogen inoculation with the Aspergillus sydowii fungus, detecting increased expression of the immune recognition gene Tachylectin 5A (T5A) in response to both parasites. Cellular immunity increased by 8.16% in copepod infections compared to controls and single Aspergillus infections. We also detected activation of cellular immunity in reef populations, with a 13.6% increase during copepod infections. Cellular immunity was similar in the field and in the lab, increasing with copepod infections and not the fungus. Amoebocyte density and the expression of T5A and a matrix metalloproteinase (MMP) gene were also positively correlated across all treatments and colonies, irrespective of parasitic infection. We then assessed the scaling of immune metrics to population-level disease patterns and found random co-occurrence of copepods and fungus across 15 reefs in Puerto Rico. The results suggest immune activation by parasites may not alter parasite co-occurrence if factors other than immunity prevail in structuring parasite infection. We assessed non-immune factors in the field and found that sea fan colony size predicted infection by the copepod parasite. Moreover, the effect of infection on immunity was small relative to that of site differences and live coral cover, and similar to the effect of reproductive status. While additional immune data would shed light on the extent of this pattern, ecological factors may play a larger role than immunity in controlling parasite patterns in the wild. Parsing the effects of immunity and ecological factors in octocoral co-infection shows how disease depends on more than one host and one parasite and explores the application of co-infection research to a colonial marine organism.
Figure 1. Two of the major sea fan parasites in the wild are (A) fungal hyphae that infect the gorgonin skeleton (see triangles), leading to purple halos shown in the field in (B); and (C) the copepod parasite infecting the mesoglea (see arrows), linked to multi-focal purple spots shown in the field in (D). Images from field samples that are representative of both field and lab samples show examples of (E) high amoebocyte density and (F) low amoebocyte density, with examples of dark pink amoebocytes in boxes. Scale bars = 0.50 μm. Photo credit: EW.
Figure 2. The clonally-replicated laboratory experiment was conducted using eight tissue samples from 10 colonies for each of the 8 treatments. The results of the experiment show (A) higher amoebocyte density during copepod infections (copepod and co-infection treatments) in comparison to the treatment with Aspergillus inoculation alone and the control. The 6- and 48-h time points are combined for each treatment as time was not a significant predictor. (B) Exposure to any type or number of parasites (i.e. the copepod, Aspergillus and co-infection treatments shown in green) induced T5A expression in the lab relative to the control. The 6- and 48-h time points are again combined as time was not a significant predictor. (C) IκB gene expression increased in the presence of any type or number of parasites in the early time point, though not significantly. IκB expression is combined across parasite treatments (copepod, Aspergillus and co-infection in green). Error bars are +/- 1SE. * denotes significance at alpha = 0.05.
Figure 3. Amoebocyte density was measured in 135 samples from 90 wild colonies sampled across 15 sites in the field. (A) Site is the most influential predictor of amoebocyte density in field samples. (B) Reproductive sea fans have elevated amoebocyte density relative to sea fans lacking ovaries or spermaries. (C) Amoebocyte density increases with copepod infection, but (D) is unchanged in fungal infections. Error bars are +/- 1SE. * denotes significance at alpha = 0.05.
Figure 4. MFPS prevalence was evaluated in 135 samples from 90 wild colonies sampled across 15 sites in the field. MPFS prevalence (A) first increases with colony size, but (B) then decreases in the very largest colonies (predicted probabilities). The resulting overall pattern is a (C) a quadratic relationship [individual shown in (A) and (B) only]. The groups in the legend, i.e. the random effect in the GLMM, are the 15 reef sites where we sampled these wild colonies (
Appendix S1: Table S4
) and colony size is in arbitrary units because it is re-scaled in the arm package (58) for use in the GLMMs.
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