Body site microbiota of Magellanic and king penguins inhabiting the Strait of Magellan follow species-specific patterns

Abstract

Animal hosts live in continuous interaction with bacterial partners, yet we still lack a clear understanding of the ecological drivers of animal-associated bacteria, particularly in seabirds. Here, we investigated the effect of body site in the structure and diversity of bacterial communities of two seabirds in the Strait of Magellan: the Magellanic penguin (Spheniscus magellanicus) and the king penguin (Aptenodytes patagonicus). We used 16S rRNA gene sequencing to profile bacterial communities associated with body sites (chest, back, foot) of both penguins and the nest soil of Magellanic penguin. Taxonomic composition showed that Moraxellaceae family (specifically Psychrobacter) had the highest relative abundance across body sites in both penguin species, whereas Micrococacceae had the highest relative abundance in nest soil. We were able to detect a bacterial core among 90% of all samples, which consisted of Clostridium sensu stricto and Micrococcacea taxa. Further, the king penguin had its own bacterial core across its body sites, where Psychrobacter and Corynebacterium were the most prevalent taxa. Microbial alpha diversity across penguin body sites was similar in most comparisons, yet we found subtle differences between foot and chest body sites of king penguins. Body site microbiota composition differed across king penguin body sites, whereas it remained similar across Magellanic penguin body sites. Interestingly, all Magellanic penguin body site microbiota composition differed from nest soil microbiota. Finally, bacterial abundance in penguin body sites fit well under a neutral community model, particularly in the king penguin, highlighting the role of stochastic process and ecological drift in microbiota assembly of penguin body sites. Our results represent the first report of body site bacterial communities in seabirds specialized in subaquatic foraging. Thus, we believe it represents useful baseline information that could serve for long-term comparisons that use marine host microbiota to survey ocean health.

Keywords: Clostridum sensu stricto; Ecological drift; Marine host microbiome; Marine sentinel microbiome; Metabarcoding; Microbial ecology; Psychrobacter; Seabird microbiota.

Figure 1. Study localities characteristics, geographic location and body sites considered.

(A) Penguin sampling sites, red mark points to Contramaestre Island, whereas black mark points to Pingüino Rey Natural Reserve. Top left inset show localities position at a continental scale. (B) Photo of Contramaestre Island with the colony of Magellanic penguin Spheniscus magellanicus. (C) Photo of Pingüino Rey Natural Reserve with the king Penguin, Aptenodytes patagonicus colony. (D) Body sites sampled (illustrated with a Spheniscus magellanicus) in this study, red bracket indicates the back, yellow indicates chest, while green points the feet. Image credit: Manuel Ochoa-Sánchez.

Figure 2. Relative abundance heatmap of the 10 most abundant bacterial families across penguin samples.

(A) King penguin body site samples. (B) Magellan penguin body site and nest soil samples.

Figure 3. Upset plot between all penguin sample types.

The pink bar highlights ASVs shared by Magellanic penguin (Sm) body sites (273); the orange bar highlights ASVs shared by king penguin (Ap) body sites (266); the green bar highlights ASVs shared by Magellanic penguin samples (190); the purple bar highlights ASVs shared by all penguin samples (139); the blue bar highlights ASVs shared by all penguin body site samples (101); the yellow bar highlights ASVs shared by penguins’ backs (82); the blue bar highlights ASVs shared by penguins’ feet (68); and the red bar highlights ASVs shared by penguins’ chests (38).

Figure 4. Alpha diversity measures, Shannon index and Faith’s Phylogenetic Diversity (PD) across penguin sample types.

Alpha diversity measures across king penguin body sites, (A) Shannon and (B) PD diversity. Alpha diversity measures across Magellanic penguin body sites and nest soil, (C) Shannon and (D) PD diversity.

Figure 5. Principal coordinate analysis applied on weighted unifrac distances across penguin samples.

(A) King penguin body site ordination. (B) Magellanic penguin body site and nest soil ordination.

Figure 6. Principal coordinate analysis applied on weighted unifrac distances to conduct penguin body site interspecfic comparisons.

(A) Interspecific comparison between all penguin body sites considered. (B) Penguins’ back comparison. (C) Penguins’ chest comparison. (D) Penguins’ foot comparison.

Figure 7. King penguin body site microbial taxa fit to Sloan Neutral Community Model.

(A) Sloan neutral community model applied to king penguin body site microbiotas. (B) Bacterial genera with most ASVs whose frequency is above predicted frequency by the neutral model. (C) Bacterial genera with most ASVs whose frequency is below predicted frequency by the neutral model.

Figure 8. Magellanic penguin body site microbial taxa fit to Sloan neutral community model.

(A) Sloan neutral community model applied to Magellanic penguin body site microbiotas. (B) Bacterial genera with most ASVs whose frequency is above predicted frequency by the neutral model. (C) Bacterial genera with most ASVs whose frequency is below predicted frequency by the neutral model.