Emergent community architecture despite distinct diversity in the global whale shark (Rhincodon typus) epidermal microbiome

Abstract

Microbiomes confer beneficial physiological traits to their host, but microbial diversity is inherently variable, challenging the relationship between microbes and their functional contribution to host health. Here, we compare diversity and architectural complexity of the epidermal microbiome from 74 individual whale sharks (Rhincodon typus) across five aggregations, globally. We hypothesised co-occurrence patterns would occur independently of diversity patterns. Whale shark aggregation was the most important factor discriminating taxonomic diversity patterns. Microbiome network architecture was similar across all aggregations with degree distributions matching Erdos-Renyi graphs. However, networks had greater modularity than expected, indicating definitive microbiome structure. In addition, whale sharks hosted 35 ‘core’ microbiome members supporting the high modularity observed in microbiomes. Therefore, while variability in microbiome diversity is high, network structure and core taxa are inherent characteristics of the microbiome in whale sharks. We suggest host-microbiome and microbe-microbe interactions which drive self-assembly of the microbiome are, in part, the result of emergent functions that support functionally redundant key core microbial members. Teaser Sentence: The skin microbiome of whale sharks has emergent co-occurrences structure despite distinct diversity patterns.

Elasmobranchs Exhibit Species-Specific Epidermal Microbiomes Guided by Denticle Topography

“…An equally important contributor to the microbial compositions are the Sphingomonodacaea population which, belonging to the Alpha-proteobacteria clade, are key contributors to initial biofilm formation and are able utilize a wide array of organic compounds 45 . Together, these two major contributors dominate the microbiome of T. semifasciata, H. francisci, and C. ventriosum, and we theorize these phyla represent core contributors and regulators to the microbiome composition of elasmobranchs, being identified in multiple shark and ray species 5,8,15,19 .…”

“…The coupling of the eukaryotic host and its respective microbial communities ("microbiome") has been reclassified as a meta-organism, representing the mutualistic dependence between a multicellular organism and its respective microbial communities 1 . Factors such as host age 2 , life history 3 , diet 4,5 , environment 6,7 , and body site 8 contribute to the composition of microbial communities to varying extents, both internally (e.g., oral, gut, reproductive tracts, etc.) and externally (integumentary system, i.e.…”