Limited transmission of microbial species among coral reef fishes from the Great Barrier Reef, Australia

Abstract

Reef fishes account for one-third of all extant marine fishes and exhibit enormous biodiversity within a highly interactive ecosystem. Yet relatively little is known about the diversity and evolution of microbial species (bacteria, viruses, and eukaryotes) associated with reef fish, even though this may provide valuable insights into the factors that shape microbial communities within vertebrate hosts as well as the extent and pattern of cross-species transmission. Through metatranscriptomic sequencing we characterised the viruses, bacteria, and single-celled eukaryotes from 128 reef fish species inhabiting Lizard Island and Orpheus Island on the Great Barrier Reef, Australia. We assessed whether microbial communities differed between islands that are separated by approximately 450 kilometres, and to what extent viruses were able to emerge in new hosts. Notably, despite strong ecological interactions in the reef environment, and the presence of the same families and subfamilies of viruses and bacteria on both islands, there was minimal evidence for the cross-species transmission of individual microorganisms among fish species. An exception was the high prevalence of the bacterial pathogenPhotobacterium damselaeamong apparently healthy cardinalfishes from both islands, indicating that these fish species are natural reservoirs within the reef system. Overall, these data suggest that reef fishes have microbial-host associations that arose prior to the formation of the Great Barrier Reef, leading to strong host barriers to cross-species microbial transmission even within a highly interactive and species-rich environment.

Diversity, evolution, and emergence of fish viruses

“…The high interconnectivity among reef fishes makes them an exceptionally powerful model system to reveal the impact of host genetic diversity on virus evolution and emergence. Reef fishes account for one-third of marine fish biodiversity, exhibit diverse trophic guilds, and typically live in close proximity ( 6 , 157 ). As a case in point, reef fishes from a community on the GBR were observed in densities of up to 150 fishes, representing 25 species in a sampling area of 3.5 m 2 , which was sustained over the course of a year ( 158 ).…”

“…As a case in point, reef fishes from a community on the GBR were observed in densities of up to 150 fishes, representing 25 species in a sampling area of 3.5 m 2 , which was sustained over the course of a year ( 158 ). Despite their connectivity, relatively high levels of sequence divergence have been observed between viruses within reef fish communities, with very little evidence for cross-species transmission ( 6 , 157 ). This indicates that high levels of genetic diversity within fish communities—reflecting the presence of fish species from many different families—should induce strong barriers to infection.…”

“…In marked contrast to reef fishes, African cichlid viromes are characterized by high levels of cross-species transmission within Lake Tanganyika ( 4 ). A notable difference between reef fishes and African cichlids is that the cichlid radiation within Lake Tanganyika occurred very rapidly, resulting in low levels of genetic divergence between fish species (e.g., differences of less than 0.03%), while reef fishes from the GBR evolved over much longer evolutionary timescales (i.e., millions of years) with barriers set in place prior to their establishment on coral reefs within the last 10,000 years ( 157 ). In addition, as the cichlid communities in Lake Tanganyika increased in diversity ~2–3 million years ago, viruses exploited a large supply of genetically similar and susceptible hosts which, in turn, increased the rate of virus diversification.…”

“…In addition, other measures such as viral abundance (e.g., the number of reads per million) and genome organization should be considered. For instance, vertebrate-associated picornaviruses are monophyletic and are clearly distinct from “picorna-like” viruses (i.e., other Picornavirales ; 1 , 2 , 6 , 157 , 165 ). Picorna-like viral polyproteins are highly divergent, such that conventional bioinformatic tools often fail to detect key domains (e.g., rhv and helicase) that are found in vertebrate-associated picornaviruses.…”

“…This, in turn, could be detrimental to native temperate and polar fishes, pushing them to extinction. For instance, virome studies have shown that smaller fishes (e.g., gobies, blennies, cardinalfishes) naturally carry a diverse array of viruses including those related to pathogens (e.g., parvoviruses and hantaviruses) ( 6 , 157 ). Another key area of future research is understanding how virome composition changes over time and assessing whether particular viruses are more prevalent during periods of fish stress or spawning.…”