Surface Topography, Bacterial Carrying Capacity, and the Prospect of Microbiome Manipulation in the Sea Anemone Coral Model Aiptasia

Abstract

Aiptasia is an emerging model organism to study cnidarian symbioses due to its taxonomic relatedness to other anthozoans such as stony corals and similarities of its microalgal and bacterial partners, complementing the existing Hydra (Hydrozoa) and Nematostella (Anthozoa) model systems. Despite the availability of studies characterizing the microbiomes of several natural Aiptasia populations and laboratory strains, knowledge on basic information, such as surface topography, bacterial carrying capacity, or the prospect of microbiome manipulation is lacking. Here we address these knowledge gaps. Our results show that the surface topographies of the model hydrozoan Hydra and anthozoans differ substantially, whereas the ultrastructural surface architecture of Aiptasia and stony corals is highly similar. Further, we determined a bacterial carrying capacity of ∼104 and ∼105 bacteria (i.e., colony forming units, CFUs) per polyp for aposymbiotic and symbiotic Aiptasia anemones, respectively, suggesting that the symbiotic status changes bacterial association/density. Microbiome transplants from Acropora humilis and Porites sp. to gnotobiotic Aiptasia showed that only a few foreign bacterial taxa were effective colonizers. Our results shed light on the putative difficulties of transplanting microbiomes between cnidarians in a manner that consistently changes microbial host association at large. At the same time, our study provides an avenue to identify bacterial taxa that exhibit broad ability to colonize different hosts as a starting point for cross-species microbiome manipulation. Our work is relevant in the context of microbial therapy (probiotics) and microbiome manipulation in corals and answers to the need of having cnidarian model systems to test the function of bacteria and their effect on holobiont biology. Taken together, we provide important foundation data to extend Aiptasia as a coral model for bacterial functional studies.

Antibiotics Alter Pocillopora Coral-Symbiodiniaceae-Bacteria Interactions and Cause Microbial Dysbiosis During Heat Stress

“…Future laboratory work should attempt to carefully manipulate associations between different coral genotypes and microbial symbiotic partners (including Symbiodiniaceae and bacteria) to move toward the generation of gnotobiotic (i.e., known-microbiome) corals for use in functional experiments. This has been shown to be feasible in cnidarian model systems such as Hydra, Nematostella, and Aiptasia (Murillo-Rincon et al, 2017;Domin et al, 2018;Medrano et al, 2019;Costa et al, 2021;Dungan et al, 2021), but is only beginning to be explored in reefbuilding corals and other cnidarians (Lin et al, 2019;Cunning and Baker, 2020;Weiland-Bräuer et al, 2020). Experiments that apply a combination of antibiotics treatments followed by targeted probiotic delivery or "microbiome recovery" treatments will yield insights into whether disturbed coral-associated bacteria communities and host stress response phenotypes can be "rescued" by the re-introduction of one or several beneficial microbes (Peixoto et al, 2017(Peixoto et al, , 2021Rosado et al, 2018;Damjanovic et al, 2019;Assis et al, 2020;Santoro et al, 2021).…”

Antibiotics reduce bacterial load in Exaiptasia diaphana, but biofilms hinder its development as a gnotobiotic coral model

“…In a recent step towards development of gnotobiotic E. diaphana , a method for bacterial depletion was reported [33, 34]. Depletion was achieved by exposure to four antibiotics with different mechanisms of action, and detection of bacteria in the treated anemones was by culture methods and PCR.…”

Exploring microbiome engineering as a strategy for improved thermal tolerance inExaiptasia diaphana

“…The failure of bacterial uptake by the host may be due to failure of the selected bacteria to be recognized as symbionts by the host, control of bacterial adhesion as described by the bacteriophage adherence to mucus model (Barr et al 2013), or founder effects whereby existing bacterial communities influence the identity of new associates (Apprill et al 2012). Further, the ciliated surface of E. diaphana may play a role in preventing bacterial adhesion (Costa et al 2021). The three-dose strategy employed in the present study was similar to previous cnidarian experiments.…”

“…Although previous studies have demonstrated that bacterial inoculation can protect E. diaphana from pathogenic infection (Alagely et al 2011;Zaragoza et al 2014), incorporation of the selected bacteria into the host microbiome was not assessed. Recently, Costa et al (2021) showed that E. diaphana is resistant to microbiome changes as transplantation of either the Acropora humilis or Porites sp. associated microbiomes failed to shift the community composition compared to Exaiptasia microbiome controls.…”

“…These approaches may address the issues of dilution and inadequate uptake of putative beneficial bacteria by coral and warrant further investigation. Furthermore, of the nearly 1000 bacteria isolated from E. diaphana (Dungan et al 2021a) and the thousands of bacterial cells they can carry (Costa et al 2021), only 12 were used in this study. More work is needed to explore the potential beneficial roles of the other bacteria, which may be possible with advances in metagenomic sequencing and the assembly of bacterial metagenome-assembled genomes.…”