Holosystemics Part VI: Fish Microbiomes, Homeostasis, and the Holobiont

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Currently unavailable obligate corallivore orangeface butterflyfish (Chaetodon larvatus) may have exhibited dietary plasticity during their putative migration through the Suez Canal to the Mediterranean (Adams 2018).

Identical processes underpin the wellbeing of the various microclimate niches (microbiomes) of organisms including corals and fish, which are economically important insofar as significant quantities of the fish consumed by humans are farmed and they can transmit zoonoses. Sea cages stress fish due to overcrowding, handling, and meaningfully polluting feeds, which leaves them susceptible to diseases, several of which have emerged over the last two decades (Fig 1.; Mougin & Joyce 2022) where wild and captive fish holobiont communities differ (Muñoz-Baquero et al. 2023). Antibiotic resistance has been acquired by many prokaryotic fish pathogens whereas several countries have banned their use and copper-based remedies for food fish. The industry has thus been forced to explore holistic methods of control which heighten natural defenses. Numerous studies are funded to investigate the mucosal microbiota of fish that inhabit their skin, gills, gut, nasal, and oral cavities which are primary routes of infection, while the environment rather than the host influences their community compositions (Lorgen-Ritchie et al. 2023). Cohorts of commensal and mutualistic microbes are central to the maintenance of an effective barrier, where destabilization and dysbiosis occur sometime before the onset of pathology. It is imperative therefore to identify biomarkers which assist early detection for timely disease-mitigating probiotic and prebiotic manipulations. If such therapies are effective in the over-disquieting milieus of mariculture, they cannot fail to enhance the vitality and survivorship of ornamental marine fish in optimized reefs or fish-only systems. Few grants are awarded to investigate fish destined for aquaria, so we necessarily simplify and present the findings of mariculture research, while the previous editorials in this series are considered foundational which support interpretation.

We cannot eradicate disease in reefs like we can in fish-only systems. Appreciation of holobiont and pathogen gene expression and the dynamics of their adaptive, biocidal, immunological, and virulence strategies remain central to the development of cures, which must respect the housekeeping commensals that become opportunistic pathogens when holobiont defenses are compromised or when fish integuments are breached. Cutting-edge perspectives have commenced to regard all microbes as opportunistic including Koch’s postulate-affirmed aetiological agents, while proposing disease originates from perturbations in microbial function which initiates homeostatic destabilization and diminished immunity (Mougin & Joyce 2022).

Fig 1. Mariculture sea cages raising seabass and sea bream off Galaxidi in Greece.

We are better placed to understand what constitutes a “healthy” population after studying the various microbial communities in the previous articles. We comprehend that diversity, richness, and evenness are vital, however from an objective standpoint it is challenging to define the exact composition that contributes to function. A cross-taxa core microbiome that supports finfish homeostasis is unlikely to exist (Lorgen-Ritchie et al. 2023). Instead Mougin and Joyce (2022) studied a specified pathogen and dysbiotic state which contributed to aetiology, diagnosis, and therapy. They theorized disease is proceeded by a loss of “healthy” prokaryotic phylotypes and their adaptive remedial competencies described as metagenomic plasticity. It is unclear if dysbiosis causes or is a symptom of disease, nevertheless three types are exemplified by a loss of beneficial microbes (i), constrained microbial diversity (ii), and the emergence of an aberrant holobiont (pathobiont; iii), all of which have discernible features (Mougin & Joyce 2022).

Around 90 percent of all seawater biomass is microscopic, and the microbiomes of its inhabitants are inextricably linked to the microbial profile of their surroundings (Edgerton et al. 2018). The gut, skin, and gills of fish have defined microbial communities yet more is known of the gut mucosa and its populations due to its importance in contagion and aetiology, and an endocrine, neuro-, and immunological association called the gut-brain axis (Rosado et al. 2022). Furthermore marine teleosts must continuously drink water to assist osmoregulation as all marine life must guard against desiccation, where pathology of the gut mucosae elicits “leaky” interstitial (intercellular) junctions (Sitjà-Bobadilla et al. 2019) which assist pathogen infiltration. Likewise the paracellular routes of marine fish gill are easier to negotiate compared with those of freshwater fish. Intestinal epithelial surfaces and their microbial consortia exhibit profound antimicrobial competences (Fouz et al. 2000) however some pathogens may be internalized by glycoprotein or actin-dependent endocytosis where they escape destruction (López-Dóriga et al. 2000; Andreoni & Magnani 2014).

It was concluded in the late 20th century that fish intestines harbored limited microflora, however less than 1 percent of microbes could be isolated and identified using the agar of the time (Amann et al. 1995) so gut mucosal microbiomes were grossly underestimated (Edgerton et al. 2018). Molecular techniques now indicate that such analysis could only detect 0.1 percent of fish gut affiliates (Zhou et al. 2014).

Numerous studies have recognized a significant perturbation of gut microbes during enteritis, although such changes are not localized because cross-holobiont communities may shift. Gut infections can transform the microbial communities of skin and gills (Legrand et al. 2018) albeit dynamic alterations in populations arise as aetiologies advance (Mougin & Joyce 2022).

The adaptive and innate immunity of higher eukaryotes will exert a more pronounced effect on the microbial communities of their microbiomes compared to corals with merely an innate response. All mucosal surfaces are flooded with compliment, oxidative bursts, antibodies, and numerous phagocytic lymphocytes.

Next-generation sequencing (NGS) techniques like the algorithm linear discriminant analysis effect size (LEfSe) identifies metagenomic biomarkers of key prokaryotic species, their gene expression and metabolism, and discriminates between microbial communities with unique profiles. That said, such technology has yet to be used in aquaculture (Segata et al. 2011, cited in Mougin & Joyce 2022). Multi“omic” approaches integrate taxonomic, metagenome, metatranscriptome, and metaproteome databases, with biomarkers of microbial networks, prokaryotic defense, and metabolism (Bass et al. 2019).

A loss of diversity in gut microflora is associated with overgrowth with a handful of species, however the phyla Fusobacteria and Firmicutes have been recognized as members of beneficial consortia. A study suggested a decline in these lineages and an increase of Proteobacteria was commensurate with disease (Miyake et al. 2020). Mycoplasma species (Firmicutes) have also been identified as a genus that is present in “healthy” populations which decline before the onset of pathology, however other studies have linked the genus Mycoplasma with pathogenesis. Cetobacterium species were found in healthy populations where they synthesise vitamin B12 and their decline was indicative of contagions, whereas proliferation of the genera Aeromonas, Shewanella, and Vibrio was redolent of pathology (Mougin & Joyce 2022).

Several studies have noticed a change in bacterial composition accompanies infections of the skin and gill. The prokaryotic genera Acinetobacter, Shewanella, and Pseudomonas were curtailed on the skin of freshwater trout during colonisation with “white spot” (Ichthyophthirius multifiliis; Zhang et al. 2018; Mougin & Joyce 2022). Changes in the biochemical profile of mucus and a declination of the genera Alteromonas, Thalassabius, and Winogradskyella and trivial blooms of Flavobacterium, Chryseobacterium, and Tenacibaculum species were associated with skin ulcerations of gilthead seabream (Sparus aurata; Tapia-Paniagua et al. 2018), whereas two further studies suggested mucosal Rubritalea species were integral to the healthy consortia of European seabass (Dicentrarchus labrax; Rosado et al. 2019a; Cámara-Ruiz et al. 2021) where the known pathogen Vibrio harveyi increased diversity (Cámara-Ruiz et al. 2021). Similarly, Stenotrophomonas, Polaribacter 4, Pseudomonas, and Rubritalea species were lost from the gills of Dicentrarchus labrax infected with Photobacterium damselae piscicida (Rosado et al. 2019a). Rubritalea species are core cross-anatomy affiliates of Dicentrarchus labrax and Sparus aurata (Rosado et al 2019b; Rosado et al. 2021) which provide carotenoids, squalene, other antioxidants and beneficial metabolites (Spanova & Daum 2011; Yoon et al. 2018). Nevertheless this genus is merely indicative of the beneficial consortia of these species (Mougin & Joyce 2022).

Oleispira species declined on the skin of Atlantic salmon (Salmo salar) infected with salmonid alphavirus (SAV) where these microbes somehow assist the saltwater acclimation (smoltification) of parr and appear to shield against pathogens in triploid fish with three copies of each chromosome (Reid et al. 2017; Brown et al. 2021) insofar as 3n is routinely induced in aquacultured salmonids to preclude wildtype crosses. The ratio of the phyla Proteobacteria to Bacteroidetes decreases in skin mucus with the onset of enteritis in yellowtail kingfish (Seriola lalandi) where such ratios maybe useful for early generic biomarkers where wild kingfish exhibit higher ratios (Legrand et al. 2019).

Proteobacterial proliferation in fish alimentary canals is a nonergonomic warning signature insofar as fish must be destroyed for analysis (Miyake et al. 2020) while Pseudomonas species have been associated with diseased Yunlong grouper (Epinephelus species; Ma et al. 2019). Waterborne Vibrionaceae correspond to populations inhabiting cultured fish, and thus the profile of planktonic bacteria appears a valuable barometer of livestock health (Kim & Lee 2017). Dysbiosis and disease has been associated with the opportunistic genera Chryseobacterium (Weeksellaceae), Flavobacterium (Flavobacteriaceae), Granulicatella (Carnobacteriaceae), Pseudomonas (Pseudomonadaceae), Streptococcus (Streptococcaceae), Tenacibaculum (Flavobacteriaceae), and Vibrio (Vibrionaceae; Llewellyn et al. 2017; Reid et al. 2017; Tapia-Paniagua et al. 2018; Zhang et al. 2018).

Quests for taxonomic biomarkers have failed to provide the necessary insight likely due to confounding serotypes, constantly evolving species and strains, species-specific interactions as well as abiotic and ecological factors (Mougin & Joyce 2022). Screening techniques must identify the entire profile of beneficial microbial communities under all types of environmental conditions for each species before such investigations yield useful findings. Too numerous to quantify variables thwart these investigations where ergonomic and efficacious molecular techniques are required.

Holistic approaches use high-throughput molecular screening to profile prokaryotic communities that propose populations are shaped by host immunity and gene expression (Wang & Loreau 2014; Kim et al. 2017) which is supported by our observations in the preceding editorials. Studies suggest that low diversity is nonindicative of dysbiosis and disease (Bozzi et al. 2021) because increments or decrements can head pathology onset (Bass et al. 2019; Mougin & Joyce 2022). Such findings redirect our attention to community shifts irrespective of prokaryotic phylotypes, diversity, evenness, and richness, while population profiles are restructured temporally by aetiology and defense (Mougin & Joyce 2022).

Functional redundancy and the identification of cross-population gene homologues or metabolic signatures within mucus may prove worthwhile biomarkers, where tools like PICRUSt cross-reference 16S rRNA databases with metagenomic function (Langille et al. 2013; Ortiz-Estrada et al. 2019). Such analysis has its limitations inasmuch as BLAST searches may unearth unexpressed/dormant genes or vestigial non-functional homologues or those that have evolved divergently to perform unpredictable roles, while databases may lack phylogenetic breadth and depth (Mougin & Joyce 2022).

Fig 3. Skin and gill metabolome analyses of seabream and European Seabass: early juveniles [EJ]; late juveniles [LJ]; juveniles [J]; mature adults [MA]; biosynthesis [Bios]; degradation/utilization/assimilation [DUA]; generation of precursor metabolites and energy [GPME], and macromolecule modification [MM]. Analyses and image courtesy of Rosado et al. 2021 and the Creative Commons Attribution License.

Microbial metabolic function fluctuates throughout disease (Ma et al. 2019) yet these vacillations may not be evident on skin (Rosado et al. 2022). Mucosal inorganic, organic, complex, simple, dissolved, and particulate carbon, amino acids, pyrimidines, glycerol, and phosphorylated compounds influence microbial communities (Fig 3.; Ritchie & Smith 1995; Rosado et al. 2021) while expression of their extracellular enzymes may facilitate designation as part of a healthy or diseased microbiota (Mougin & Joyce 2022). Differential gene expression was used to discriminate between diseased and non-diseased goldfish (Carassius auratus) like homologues associated with bacterial motility, chemotaxis, secretion systems, signaling, and toxins (McBride & Nakane 2015; Lasica et al. 2017; Li et al. 2017; Pérez-Pascual et al. 2017; Cherrak et al. 2019; Santos et al. 2019). Secretion systems assist the intramacrophage survival of pathogens (Zhang et al. 2016) while genes encoding virulence determinants are often encoded on horizontally transmissible nucleic acids such as pathogenicity islands, plasmids, or they may be integral to lysogenic prophage, all of which may be useful biomarkers of disease. Alternatives may include immune signatures such as those that support metagenomic plasticity or those induced by danger molecule signaling known as DAMPs (Mougin & Joyce 2022; Aslett 2024a). Fish gut mucosae is flooded with antibodies (immunoglobulins; Igs), hydrolytic enzymes (Perdiguero et al. 2019), and inflammatory response-induced lymphocytes (Scapigliati et al. 2018). The granulocytes neutrophils, monocytes, and eosinophils contain myeloperoxidase and peroxidase enzymes that combine the halogen ions chloride (Cl), bromide (Br), and iodide (I) with hydrogen peroxide (H2O2) to form potent toxins that destroy tumors and pathogens (Flerova & Balabanova 2013), and perforin and granzyme are toxic to cells (cytotoxic; Hlongwane et al. 2018). Fish express interferon type-1 (INF-1) which is a multifunctional cytokine associated with the suppression of viral virulence (Zhang & Gui 2012), while myxovirus resistance (Mx) proteins belong to a family of guanosine triphosphatases (GTPases) which assemble into intracellular antiviral machines (Tretina et al. 2019). Antimicrobial peptides (AMPs) are pervasive and integral to finfish, coral, and microbial defense (Shabir et al. 2018; Valero et al. 2019), while the finfish IgM tetramer is a common antibody of the skin, gut and gill mucosae that marks antigens and foreign invaders with phagocytosis-inducing opsonin (Mashoof & Criscitiello 2016).

Any method for monitoring maricultured specimens must be non-invasive, non-stressful and convenient, such as ventral or flank scrapes and/or water analysis, however the latter appears to promote inconsistency (Mougin & Joyce 2022). Perhaps investigations of water are only useful during an active infection with high planktonic loads.

We cannot make progress unless we unravel the mechanisms that underpin eubiosis and dysbiosis and ascertain which comes first: microbial community perturbations or disease (Mougin & Joyce 2022). Remarkably this area of research seems less explored than the microbiomes of corals and the holobiont network that supports and reinforces coral homeostasis and symbiosis. Nevertheless, what we have learnt from corals may be applicable.

Corals sift and selectively nurture residual symbionts and/or recruit them from the environment during abiotic disruptions in accordance with the microbial flexibility hypothesis. The prokaryotic holobiont communities of corals alter gene expression where metagenomic plasticity facilitates shifts in their population dynamics in the face of mild or moderate stress. Replete microbiomes demand extensive purging to accommodate recruitment and restructuring yet survival necessitates timely reversion. It is advised that dysbiosis is a natural and intended response for corals to a chronic stressor that exceeds the mitigating capacity of their microbes. Common symptoms of fish disease include surplus mucus and/or shedding of gut epithelium seen as a white stringy anal discharge. It is likely such responses are immunological and instigated by the host, like a raised temperature in human infections or coral bleaching, because mucosal sloughing also rids the fish of surface microbes. Signatures likely arise in fish mucus in response to pathogenic colonization, or after significant flushing to re-establish a healthy community, yet it may be too late to use them for early detection (Boilard et al. 2020; Mougin & Joyce 2022; Aslett 2024b).

Studies have focused on the bacterial affiliates of fish because they are likely candidates for mitigating illness and expediting recovery, however microeukaryotes and Archaea are present in fish holobionts that may manufacture detectable biomarkers. Viruses including bacteriophage are present which constitute the virome, which mobilize nucleic acid and may thus transform the virulence or environmental compliance of their lysogenic hosts. Alas, lytic bacteriophages mutate too frequently to be used as therapies to destroy pathogens, yet they may be engineered while they retain an aptitude for shaping and transforming microbial populations (Mougin & Joyce 2022). Notwithstanding, self-assembling virus-like polymers composed of viral protein coat monomers have been used as efficacious vaccines (Thiéry et al. 2006).

Next time we dedicate part VII to the innovative research of Gallet and collaborators (2023) who simulated in vitro blooms of toxigenic cyanobacteria while screening the symbiomes, pathobiomes, and metabolomes of healthy, eutrophication, and bloom-exposed fish.


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