Holosystemics Part VIII: Fish Holobionts, Aetiology and the Pathobiome

by | Jul 10, 2024

Our understanding of disease is evolving because many do not originate from the exploits of a primary pathogen, which do not merely interact with the host and its immune system, but with the multipartite holobiont and its immediate surroundings. Illnesses appear a consequence of a dynamic process whereby microeukaryotic and prokaryotic symbionts, commensals, and their viruses, initially attempt to outcompete and eradicate invading microorganisms by liberating antimicrobials and modifying their community compositions and metabolism. Cellular trauma that exceeds their restorative potential demands participation of adaptive and innate immunity. Host defense transforms the conditions within its microbiomes to curtail spread and purge disease-causing agents, which leads to transitory and intended states of dysbiosis. The pathobiont is the consequence of the host’s altered constituent physiology and its now hostile microniche (pathobiome), and its modified community and metabolic function (pathobolome) which we hitherto called disease (Bass et al. 2019).

Fig 1. A color variant of the percula clownfish (Amphiprion percula) stricken with Brooklynella cf. hostilis with a moribund posture comprising “clamped” fins. Image courtesy of Alex Cole ©, Meridian, Idaho, USA.

The term symbiome refers to a microniche and its microbial community including microeukaryotes, prokaryotes, and their viruses which may be benign, mutual- or antagon-istic, whereas skin-residing mutualists are often referred to as epi-symbionts. Interactions may be short or long lived, where pathobiome development is often gradual and advocates novel mitigating approaches. Investigations must consider abiotic and biotic contributions insofar as pathobiomes may arise from unfavorable conditions and invasions of environmental microbes (Bass et al. 2019), while commensals like Brooklynella hostilis may proliferate and aggressively erode gill and skin (Fig 1.; Rohde 1932; Lom & Corliss 1971; Noga 2010).

Fig 2. A post-mortem example of freshwater kuria labeo (Labeo gonius) exhibiting epizootic ulcerative syndrome (EUS) caused by the fungus-like chromist Aphanomyces invadans which is a disease epitomizing hyphae-derived host-specific aetiologies, site-specific ulcerations, petechial hemorrhages, and tail erosion. Nevertheless A. invadans is constrained to hyposaline or freshwater (Blazer, personal communication).

Fish pathogens include microorganisms from every kingdom where an established lesion is an ecological niche where a consortium of microorganisms exploit a range of nutrition, whereas abiotic environmental impacts and immune subversion may recrudesce dormant aetiological agents (cryptic pathogens; Bass et al. 2019). A consortium may act synergistically to intensify pathology, like the infamous coinfection of Atlantic menhaden with Pfiesteria species of dinoflagellate and the fungi-like chromist Aphanomyces invadans from 1996 to 1997 in Chesapeake Bay (Fig 2.; Blazer et al. 2016), yet equally, multiple contagions can prove aetiologically attenuating.

Bacterial quorum quenching degrades the agenda-orchestrating signaling autoinducers of other prokaryotes, or the complementary metabolites of a few symbiome or pathobiome affiliates may be shared (Bass et al. 2019). Several pathogens are recognized inhabitants of “healthy” microbiomes yet increases of host apoptosis or necrosis trigger their logarithmic growth and community destabilization beyond a predetermined threshold. Such disproportionate proliferation within a finite niche forces taxa extinction and a loss of diversity. Inter-symbiont horizontal gene transfer arms benign microbes with virulence factors and frequencies are elevated by stress (Bass et al. 2019).

The “Anna Karenina” principle proposes the microbial compositions of dysbiotic organisms vary more than those of “healthy” (Zanefeld et al. 2017, cited in Bass et al. 2019) however in stark contrast to many studies, a succession of limited microbial taxa and a dip in diversity has been associated with mitigation (Webster et al. 2019, cited in Lorgen-Ritchie et al. 2023). Certain prokaryotes confer resistance to specified disease-causing agents where these lineages were enriched in frog skin from pathogen-infested environments yet appeared nominally in pathogen-free milieus (Walke et al. 2017, cited in Bass et al. 2019). Probiotic manipulations are tangible goals for corals and fish and their immediate surroundings however we must exercise caution. The microbiomes of “healthy” corals are unaffected by beneficial microbes (BMCs; Santoro et al. 2021) yet attempting to exclude perceived pathogens from symbiomes is hazardous insofar as there are significant gaps in our understanding (Bass et al. 2019).

Fig 3. Holobiont/environmental dynamics. Image courtesy of Lorgen-Ritchie et al. 2023 and the Creative Commons Attribution Licence (CC BY). http://creativecommons.org/licenses/by/4.0/

The gut of zebrafish includes 15 fungi belonging to the phyla Ascomycota, Basidiomycota, and Zygomycota, yet the communities of wild and captive fish a dominated by contrasting kinds (Siriyappagouder et al. 2018), while fungi modulate the digestion, immunity, and hormones of gilthead seabream (Sparus aurata; Naya-Català et al. 2022). The communities of planktonic microbes in both recirculating and sea cage environments are shaped by abiotic and biotic factors such as the weather and husbandry in dynamic flux. Finfish fry adaptive and innate immunity are not primed and external and internal microbes do not colonize until after hatching and first feeds, where microbe-derived bacteriocins, fungicides, antimicrobial peptides (AMPs), viruses/bacteriophage, and immunity commence to structure microbial populations (Lorgen-Ritchie et al. 2023). Cell surface receptors encoded by cell germlines may play a central role in recruitment and winnowing which are likely tissue-specific, and akin to corals there is evidence of sophisticated “crosstalk” between microbes and host immunity (Kelly & Salinas 2017).

Unless infected vertically in gamete mucus, fish are only colonized by immunity-evading/resilient environmental microbes (Lorgen-Ritchie et al. 2023) whereas host genotype influences prokaryotic recognition, sifting, and the biochemical composition of its microclimates (Spor et al. 2011). Host genotype and epigenetic modification may have a profound effect on microbial communities which is impacted by cellular metabolites, while invertebrates can exhibit lasting transgenerational immunity. Microbiomes may be shaped in aquaculture using targeted environmental conditioning (Lorgen-Ritchie et al. 2023) inasmuch as the ratios of organics to inorganics determines heterotrophy versus autotrophy, where the former can overgrow biofilms or outcompete planktonic nitrifying autotrophs responsible for detoxification of ammonia (Hovanec, personal communication 2019). Water turnover, degas/regas, and purification has a direct impact on microbes which become microbiome affiliates, whereas the introduction of healthy animals can act as welcome inoculants. System and animal fitness are thus interrelated where function or malfunction are expedited on a sliding scale in dynamic equilibrium. Defining optimal conditions is challenging in aquaculture due to the variety of methodologies, while parameter manipulation remains child’s play in recirculating systems (Lorgen-Ritchie et al. 2023).

Pathogens such as Vibrio and Photobacterium species (Vibrionaceae) proliferate in response to increased temperature while circadian rhythm and thus homeostasis are influenced by photoperiod. Biofloc technology is used in recirculating aquaculture systems (RAS) to maintain healthy nitrifying communities which in turn supports livestock defense (Lorgen-Ritchie et al. 2023). Feeding the inhabitants of an ornamental tropical marine fish-only systems several times per day has an analogous effect. Heavy feeds are not uncommon in aquaculture yet they devastate reefs, while forms of sterilization may prove harmful, and biofouling exerts impacts (Lorgen-Ritchie et al. 2023). Detrital purging is thus important in all recirculating systems, however cleaning deep sand beds and “plenums” is risky.

A “healthy” microbiome must respond and adapt to varying conditions, support host homeostasis, and provide resilience to disease, where function and the metabolome is more vital than phylogeny. Compliant populations contribute to host phenotypic plasticity, whereas stress-mediated host cortisol impacts community dynamics and may be used as a biomarker (Lorgen-Ritchie et al. 2023).

Dysbiosis and rebiosis occur during smoltification of Atlantic salmon a week after holobionts transition from fresh- to salt-water, where contrasting populations are established by week four (Lorgen-Ritchie et al. 2021). Chemotherapeutic antimicrobial agents have resulted in microbiome destabilization and an escalation of amoebic gill disease (AGD; Slinger et al. 2021) caused by a complex and somewhat interchangeable consortium (Rozas-Serri 2019).

High-throughput amplicon sequencing has been used to profile microbial communities and metabolomes, however it is limited inasmuch as databases of microbiome affiliates are underpopulated, where many such gene sets are transcriptionally inactive or downregulated. Holistic“omic” approaches like metagenomics, metatranscriptomics, metaproteomics, and metabolomics combined into multi-omics and “hologenomics” attempt to elucidate and contextualise the interactions of cross-anatomy cross-environmental genes, their products, and those of the host, which rely upon extensive sampling and yet to be established bioinformatics. Innovative exploitation of hologenomics will likely highlight the contrasting and alike functional dynamics and redundancy of fish holobionts (Lorgen-Ritchie et al. 2023).

Gnotobiotic animals are reared sterile in a sterile environment which may be used to clarify the impact of a single microbe or cohort (Zhang et al. 2020) where studies have elucidated how gut microbiota exert vital immunological and morphological impacts in the intestines of developing cod (Gadus morhua; Vestrum et al. 2022). Waterborne bacteria inoculated into the gut of germ-free zebrafish expressed 212 genes 59 of which were also detected in mouse intestines which is redolent of evolutionary conservation; however teleostean recruitment is more selective than murine (Murdoch & Rawls 2019). 59 genes were also differentially expressed in the gut of sterile zebrafish infected with Pseudozyma species of yeast exemplifying the proficiency of interkingdom taxa in metabolism and immunity, yet no changes were observed in exposed conventionally reared fish (Siriyappagouder et al. 2020). The phylogenetic lineages of fish gut inoculums became microbiome affiliates, yet their community compositions consistently aligned with the species of their host. These studies suggest such strategies may be safely used for restorative therapies (Lorgen-Ritchie et al. 2023).

Recombinant, “knockout” and “knock-in” genetic approaches whereby organisms are genetically modified unravel the intricacies of microbial consortium dynamics. Genetic modification of rainbow trout (Oncorhynchus mykiss) limited their mucosal titres of secretory immunoglobulin T (sIgT) which are crucial for pathogen suppression and microbiome stability. sIgT mutants exhibited a negligible IgM response, were dysbiotic, and experienced cellular trauma and inflammation compared with wildtype (Xu et al. 2020). Finfish clones offer consistent microbiomes for comparative studies, whereas the renaissance of in vitro bacterial culture provides opportunities to study and characterize otherwise rare prokaryotic consortia which populates and consolidates metaproteomic, metagenomic, and metabolomic databases (Lorgen-Ritchie et al. 2023).

Manipulations exploiting beneficial microbes for fish (BMFs) must be cost effective and comprise stable species and strains, that may be prominent key taxa implicated in disease mitigation or immunity, homeostatic endurance, or rebiosis which will likely be a handful of taxa or discrete subspecies. Cyst-forming heterotrophic microbes are stable in bottles yet they outcompete and overgrow autotrophic nitrifiers which may result in detectable nitrite (Hovanec, personal communication 2019).

Probiotics are diets comprising live microbes that elicit competitive exclusion, while prebiotics contain vital nutrients know to stimulate the proliferation of “good” bacteria. These therapies promote synergy as combined synbiotics (Lorgen-Ritchie et al. 2023) whereas fish immunostimulation using household and commercial products is explored in Aslett 2023c.

Therapies should be timed to optimize efficacy throughout critical developmental stages such as hatching, larval rearing, saltwater acclimation, or during heat and/or hypoxia-induced stress or dysbiosis, which warrants further investigation. Pro- and pre-biotics are conventionally dietary, while manipulative cultures can be applied directly to water in recirculating systems to transform mucosal populations. However this discipline is in its infancy and random inoculations of bacterial cultures will most likely prove harmful, whereas studies of fungal, viral and microeukaryotic symbionts present novel remedial approaches. Consortium-specific AMPs represent an innovative therapy which should strengthen commensals/mutualists whilst precluding pathogens and resistance, where function rather than phylogeny appear decisive (Lorgen-Ritchie et al. 2023).

Next we examine the dynamics of the skin mucosal microbiome of juvenile seabass throughout challenges with wild pathogens thanks to the discerning research of Rosado and allies from 2022.

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