Tenacibaculosis Disease: Diagnosis, Treatment, and Control

Marine aquaculture constantly faces threats from diseases affecting farmed species. One of the most significant is Tenacibaculosis, primarily caused by Tenacibaculum maritimum, a pathogen that leads to severe economic losses due to mass mortalities.

Tenacibaculosis is an ulcerative disease affecting a wide variety of marine fish species. It is characterized by external lesions on the skin and fins of infected fish, which can rapidly progress and result in death.

Despite advances in understanding Tenacibaculosis over recent decades, it remains a major challenge for the aquaculture industry. The bacterium’s ability to form biofilms, its antibiotic resistance, and the lack of effective vaccines complicate its control.

This article explores in depth the most relevant aspects of Tenacibaculosis and its primary causative agent, Tenacibaculum maritimum, covering topics such as taxonomy, pathogenesis, diagnosis, treatment, and prevention strategies. Additionally, we review the latest research advancements and future perspectives for controlling this disease.

Impact on Marine Aquaculture

Tenacibaculosis, also known as Yellow Mouth Disease (Wassmuth et al., 2024), primarily caused by the bacterium Tenacibaculum maritimum, significantly impacts the global aquaculture industry, affecting both fish health and the profitability of fish farms (Småge et al., 2016a; Lopez et al., 2022; Mabrok et al., 2023).

Tenacibaculosis causes high mortality rates in farmed fish populations, resulting in considerable economic losses for the aquaculture industry (Lopez et al., 2022; Småge et al., 2016a; Wassmuth et al., 2024; Småge et al., 2016b). For instance, losses attributed to Yellow Mouth Disease, a form of Tenacibaculosis, have been estimated at $1.6 million annually for a single company (Wassmuth et al., 2024). The associated economic losses include:

• Mass mortalities during critical farming stages.
• Reduced quality of the final product.
• Increased costs for treatments and health management.

Fish Species Affected by Tenacibaculosis

Tenacibaculosis, or Yellow Mouth Disease, affects various farmed fish species worldwide (Bridel et al., 2020; Mabrok et al., 2023). Among the most affected species are:

• Atlantic Salmon (Salmo salar): Tenacibaculosis poses a significant challenge for Atlantic salmon farming due to mortality and antibiotic usage (Småge et al., 2018). Outbreaks have been reported in regions including Chile and Canada (Småge et al., 2016a; Mabrok et al., 2023). Other species of Tenacibaculum, such as T. finnmarkense and T. dicentrarchi, have also been isolated in salmon outbreaks (Småge et al., 2018). Stressful conditions, such as handling and transport, are associated with outbreaks, particularly affecting juveniles (Wassmuth et al., 2024).
• European Seabass (Dicentrarchus labrax): This species is susceptible to Tenacibaculosis, as reported in France, Turkey, and Egypt (Yardimci y Timur, 2015; Småge et al., 2016a; Mabrok et al., 2023). Clinical signs include skin ulcers and mouth erosion. Research by Ferreira et al., (2024) highlights the critical role of the infection route in disease manifestation.
• Turbot (Scophthalmus maximus): This species is affected by T. maritimum, particularly in Spain. Notably, the only commercial vaccine against T. maritimum is for this species.
• Sole (Solea solea and Solea senegalensis): Both common sole and Senegalese sole are susceptible. T. maritimum and other species of the genus have been isolated from farmed sole in Spain.
• Gilthead Seabream (Sparus aurata): Reports of T. maritimum affecting gilthead seabream have emerged from Egypt.
• Rainbow Trout (Oncorhynchus mykiss): Although less common, Tenacibaculum species (T. dicentrarchi and T. finnmarkense) have been identified in farmed rainbow trout in Chile (Avendaño-Herrera et al., (2020).
• Pufferfish (Takifugu rubripes): T. maritimum has been isolated from diseased pufferfish in Japan.

Other affected species include Japanese red seabream (Pagrus major), black seabream (Acanthopagrus schlegeli), lumpsuckers (Cyclopterus lumpus), and mullet (Mugil capito), as well as ornamental fish like Picasso triggerfish (Rhinecanthus aculeatus), black damselfish (Neoglyphidodon melas), and humphead wrasse (Cheilinus undulatus). Clayton y Seeley (2019) cite that the bacterium Tenacibaculum maritimum causes necrotic skin lesions in sand tiger sharks.

General Characteristics of Tenacibaculum maritimum

Taxonomy

Tenacibaculum maritimum is a Gram-negative, filamentous, gliding bacterium from the Flavobacteriaceae family. Its taxonomic classification is as follows:

• Domain: Bacteria
• Phylum: Bacteroidetes
• Class: Flavobacteriia
• Order: Flavobacteriales
• Family: Flavobacteriaceae
• Genus: Tenacibaculum
• Species: Tenacibaculum maritimum

T. maritimum is the type species of the genus Tenacibaculum. The genus Tenacibaculum is found within the clade Tenacibaculum-Polaribacter in the family Flavobacteriaceae of the phylum Bacteroidetes. The genus Tenacibaculum includes several pathogenic species for marine fish. Originally, T. maritimum was classified as Flexibacter maritimus, but it was reclassified into the genus Tenacibaculum in 2001. Other species within Tenacibaculum include T. ovolyticum, T. discolor, T. soleae, T. dicentrarchi, T. finnmarkense, T. singaporense, and T. piscium.

Escribano et al., (2024) published the complete genome sequence of the T. maritimum SP9.1 strain, which represents the emerging serotype O4. The genome provides valuable information on the genetic basis of virulence and adaptation, complementing the existing data for the O1 serotype.

Natural Habitat of Tenacibaculum maritimum

The bacterium Tenacibaculum maritimum is primarily found in marine environments and has been isolated from various sources, including sick fish, water, sediments, and aquaculture tank surfaces.

T. maritimum has the ability to form biofilms on various surfaces, including aquaculture tanks and fish mucus. These biofilms may serve as reservoirs for the bacterium and facilitate its persistence in the environment. The outer membrane vesicles (OMVs) produced by the bacterium appear to play an important role in the formation of these biofilms (Escribano et al., 2023).

On the other hand, scientists have suggested that other marine organisms may act as reservoirs or vectors for T. maritimum. For example, Småge et al., (2016a) and Mabrok et al., (2023) report that the bacterium has been found in sea lice (Lepeophtheirus salmonis). It has also been suggested that jellyfish blooms (Dipleurosoma typicum and Phialella quadrata) could serve as sites for colonization and sources of infection by Tenacibaculum (Småge et al., 2017; Mabrok et al., 2023).

Pathogenesis of Tenacibaculosus

The pathogenesis of tenacibaculosis, a disease primarily caused by the bacterium Tenacibaculum maritimum, is a complex process that is not yet fully understood. However, Småge et al., (2016b) reported the presence of Tenacibaculum finnmarkense sp. nov. in the skin lesions of a sick Atlantic salmon in Norway; and Småge et al., (2018) demonstrated the induction of tenacibaculosis in salmon smolts. On the other hand, Nowlan et al., (2021) induced tenacibaculosis (yellow mouth disease) in Atlantic salmon through exposure to T. dicentrarchi, suggesting that other species of Tenacibaculum may also cause the disease.

The scientific literature has identified several factors and mechanisms that contribute to the development of the disease. Below is a summary of the pathogenesis of tenacibaculosis:

• Initial Adhesion: The first step in pathogenesis is the adhesion of T. maritimum to the fish surfaces. Unlike many bacteria, T. maritimum does not have structures like pili, flagella, or fimbriae for adhesion. Instead, it uses non-specific mechanisms such as hydrophobic and ionic interactions. It has also been shown that the outer membrane vesicles (OMVs) of T. maritimum promote adhesion to surfaces. The ability to form biofilms on fish surfaces is crucial for the persistence and transmission of the bacterium.

• Colonization and Spread: After adhesion, T. maritimum colonizes the fish tissues. The bacterium spreads across the skin surface and can invade deeper layers, including the dermis and, in some cases, the hypodermis. The bacterium multiplies rapidly in the host tissues. The sliding motility of T. maritimum plays an important role in colonization. Non-sliding isolates of T. maritimum are avirulent in immersion challenges in fish.

• Tissue Damage: The combined action of enzymes and toxins produces tissue damage characteristic of tenacibaculosis. This includes:
  • Ulcerative and Necrotic Lesions: The skin is the primary site of injury, with ulceration and necrosis of tissue.
  • Mouth Erosion: The mouth may also be affected, with erosion and hemorrhages. Wynne et al., (2020) reported that yellow mouth disease is associated with a significant dysbiosis in the microbial community of the Atlantic salmon’s oral cavity, and a significant increase in Tenacibaculum species, with T. maritimum being the most abundant.
  • Fin and Tail Necrosis: The fins and tail may show signs of necrosis and rupture.
  • Inflammation: While a lack of inflammatory markers has been reported in some cases, an inflammatory response is observed around muscle cells. In cases where there is coexistence with nematocysts, damage and pits are observed, suggesting tissue loss.

• Host immune response: The host fish responds to infection with an immune response, but T. maritimum has mechanisms to evade or suppress this response. Escribano et al. (2023) reported that Tenacibaculum maritimum, the etiological agent of tenacibaculosis in marine fish, constitutively secretes extracellular products (ECPs) containing protein. These bacterial extracellular products (ECPs) can inhibit the production of reactive oxygen species in leukocytes. It has also been observed that, at low concentrations, the ECPs stimulate the production of these reactive species, but at higher concentrations, they suppress them, suggesting the ability of T. maritimum to cope with the host’s phagocytic response.

• Predisposing factors: Several factors can predispose fish to tenacibaculosis, including:
  • Stress: Stress due to handling, transport, or unfavorable environmental conditions can increase fish susceptibility.
  • Water temperature: Water temperature plays a key role in the presence of T. maritimum. The bacterium is mesophilic, meaning it grows well between 15 and 34°C. Higher temperatures are generally associated with increased prevalence and severity of tenacibaculosis. However, outbreaks have also been recorded in winter, suggesting that other environmental and management factors may also influence it.
  • Concurrent infections: Co-infection with other pathogens can increase the severity of the disease. The presence of nematocysts (from jellyfish) also seems to exacerbate the infection.
  • Cultivation conditions: Water quality and tank conditions can influence the spread of the disease.

In summary, the pathogenesis of tenacibaculosis is a multifactorial process involving adhesion, colonization, enzyme and toxin production, immune evasion, and tissue damage. Understanding these mechanisms is essential for developing effective strategies to prevent and control the disease in aquaculture.

Diagnosis of Tenacibaculosis

Diagnosing tenacibaculosis, or “yellow mouth disease,” can be challenging due to the diversity of symptoms and the possibility of mixed infections with other pathogens. However, several methods and procedures are used to diagnose the disease. Below are the main diagnostic methods described in the scientific literature:

Clinical Signs

The initial diagnosis is often based on the observation of characteristic clinical signs of tenacibaculosis. These signs include:

• Ulcerative and necrotic lesions on the skin: These are the most common lesions, with ulcers and necrosis on the skin surface. The lesions may vary depending on the Tenacibaculum species involved, with T. maritimum associated with lesions on the body and caudal fin, while T. dicentrarchi is related to lesions on the head and snout.
• Mouth erosion: The mouth may present erosion, hemorrhages, and other lesions.
• Necrosis and fraying of fins and tail: Fins and tail may show signs of necrosis, fraying, and rupture.
• Paleness of internal organs: In some cases, paleness of internal organs may be observed.
• Presence of filamentous bacteria: Large amounts of filamentous bacteria can be observed in the affected areas.

It is important to note that these clinical signs may be similar to those caused by other pathogens, which complicates accurate diagnosis based solely on clinical observation. For example, the same symptoms may be associated with other Tenacibaculum species. Additionally, co-infections may present signs that are difficult to differentiate, as it is not clear which pathogen is responsible for each sign of infection.

Microscopic Examination

Microscopic examination of affected tissues can reveal the presence of filamentous, typically gram-negative, bacteria associated with the lesions. Histopathological studies show detachment of the dermis and epidermis, hyaline degeneration, and necrosis in the musculature. An inflammatory response around muscle cells can also be observed. Scanning electron microscopy (SEM) can reveal the presence of filamentous bacteria in the dermis and on the scales.

Isolation and Culturing

Isolation and culturing of T. maritimum from diseased fish samples is an important step to confirm the diagnosis.

• Specific Culturing Media: The use of specific media such as FMM agar or media supplemented with antibiotics is essential for isolating T. maritimum. Marine agar (MA) is also used to recover and identify Tenacibaculum species. Tenacibaculum growth is not favored on non-marine agar.
• Colony Characteristics: T. maritimum typically forms flat, pale yellow colonies with irregular edges on FMM agar, and round, yellow colonies on marine agar.
• Limitations of Traditional Methods: Traditional microbiological isolation and identification methods may require extended periods to obtain an accurate diagnosis, which can lead to high fish mortality.

Biochemical and Phenotypic Tests

Biochemical and phenotypic tests can help identify T. maritimum. These tests include colony morphology characterization and API ZYM and API 50 CH tests, among others. However, API results may vary due to several factors. Properties such as Congo red absorption, which is characteristic of T. maritimum compared to other Tenacibaculum species, can also be evaluated.

Molecular Methods

Molecular methods have become increasingly important for rapid and specific diagnosis of T. maritimum. These methods include:

• PCR (Polymerase Chain Reaction): PCR protocols are used for the specific detection of T. maritimum. Several PCR primers and probes have been described to amplify T. maritimum specific genes. Techniques such as nested PCR and multiplex PCR (mPCR) can also be used.
• RT-PCR (Reverse Transcriptase Polymerase Chain Reaction): This technique is used to detect T. maritimum RNA, allowing detection of the pathogen even when present in small amounts.
• PCR-ELISA (PCR-Enzyme-Linked Immunosorbent Assay): This technique combines PCR amplification with a serological procedure to enhance detection specificity.
• RT-PCR-EHA (Reverse Transcription PCR Enzyme Hybridization Assay): Similar to PCR-ELISA, this technique uses enzyme hybridization for detection.
• Multilocus Sequence Analysis (MLSA): Sequencing housekeeping genes for epidemiological studies and distinguishing T. maritimum from other Tenacibaculum species. It can also reveal lineages among pathogenic and environmental strains.
• DNA Microarrays: These allow rapid pathogen detection with higher specificity.
• Serotyping: Serotyping, involving identification of T. maritimum serotypes through serological tests (slide agglutination, dot-blot, and immunoblotting) with specific antisera, can be useful for epidemiological studies. Up to four serotypes of T. maritimum have been described, which complicates the development of species-specific vaccines.
• MALDI-TOF MS (Matrix-Assisted Laser Desorption/Ionization Time-of-Flight Mass Spectrometry): MALDI-TOF MS was used by Bridel et al. (2020) for rapid species identification of Tenacibaculum and for epidemiological studies. This technique can identify subtle differences between strains based on ribosomal protein profiles and other proteins. By combining multiple polymorphic biomarker ions, MALDI-types (MT) and MALDI-groups (MG) of different strains can be identified.

It is important to highlight that, due to the diversity of available methods, it is essential to use a combination of approaches for accurate diagnosis of tenacibaculosis, including clinical observation, bacterial isolation and culturing, biochemical tests, molecular methods, and serological and genomic analyses.

Treatment and Control of T. maritimum

The treatment and control of Tenacibaculum maritimum, the causative agent of tenacibaculosis, is complex and multifaceted. Currently, the treatment and control rely on a combination of measures, including the use of antibiotics, disinfectants, environmental modifications, and, in some cases, vaccination.

Antibiotic Treatment

Antibiotics are one of the main tools used to treat tenacibaculosis. The susceptibility to different antibiotics varies depending on the strain of T. maritimum and the antimicrobial agent used.

In vitro studies have shown that several strains of T. maritimum are resistant to oxolinic acid but susceptible to amoxicillin, nitrofurantoin, florfenicol, oxytetracycline, and trimethoprim-sulfamethoxazole. Some strains also show resistance to enrofloxacin and flumequine.

Other studies have found that strains of T. maritimum are sensitive to erythromycin, cephalotin, ampicillin, and chloramphenicol, but resistant to ofloxacin and tetracycline.

It is important to note that in vitro test results do not always correlate with in vivo antibiotic efficacy, which can complicate treatment. Therefore, the choice of antibiotic and dosage should be determined by a veterinary specialist. The excessive use of antibiotics can lead to the emergence of resistant strains, which is a significant issue in aquaculture.

Disinfectants

Surface disinfectants administered by immersion can be effective as a preventive or prophylactic measure. However, the effectiveness of these disinfectants may vary, and their use should be part of an integrated disease control plan.

Modification of Environmental Conditions

Water temperature is an important factor in the development of tenacibaculosis. Warmer temperatures generally increase the prevalence of the disease, with an optimal growth range for T. maritimum between 15-30°C. Lowering the water temperature and salinity may reduce the mortality associated with tenacibaculosis, although some studies have not found a significant effect of freshwater treatment on the presence of the bacteria.

Maintaining optimal breeding conditions, including appropriate stocking densities, good feeding, and preventing mechanical damage to the skin and mucous membranes of the fish, can reduce susceptibility to infection.

It is important to note that exposure to suboptimal temperatures may suppress the immunity of the fish, increasing disease prevalence.

Vaccination

Efforts to develop a vaccine against Tenacibaculum maritimum have been extensive but with variable results and significant challenges. Although progress has been made in understanding the bacteria and its pathogenesis, the development of an effective vaccine remains an active area of research.

Key efforts and challenges in vaccine development:

• Commercial Vaccine for Turbot: The only commercially available vaccine for T. maritimum is for turbot (Scophthalmus maximus), specifically the LPV1.7 serotype O2 strain. This vaccine is administered through a bath for fish weighing 1-2 g, followed by a booster injection when the fish reach 20-30 g. The survival rate of the challenged fish after bath immunization was approximately 50%, and it increased to >85% after the booster injection. The systematic application of this vaccine in some turbot farms has decreased the prevalence of tenacibaculosis.

• Difficulties for Other Species: The turbot vaccine is not effective in preventing tenacibaculosis in other fish species, such as Atlantic salmon. This indicates that the immune response is species-specific, and vaccines tailored to each type of fish are needed.

• Antigenic and Genetic Diversity: The great antigenic and genetic variability among T. maritimum strains makes it difficult to select candidate strains for vaccine development. Up to four different serotypes of T. maritimum have been identified, suggesting that a vaccine targeting one serotype may not be effective against others.

• Focus on Lipopolysaccharides (LPS): Some studies suggest that lipopolysaccharides are the main protective antigens of this pathogen. However, the variability in LPS among different strains makes the development of a universal vaccine difficult.

• Inactivated Whole Cell Vaccines: Inactivated whole-cell vaccines with oil adjuvants have been tested, but with contradictory results. While these vaccines can generate an antibody response in Atlantic salmon, they do not always provide significant protection against the disease. For example, a study in Canada using isolates from that region did not manage to protect the fish under challenge conditions.

• Need for Adjuvants: Some studies indicate that the use of adjuvants is necessary to demonstrate protection against T. maritimum in Atlantic salmon. However, some adjuvants may cause side effects, such as melanin formation with granulomas and cysts, which can affect the growth and feeding of the fish.

• Challenge Models: The lack of repeatable and reliable challenge models has been a barrier in the development of vaccines for T. maritimum. Improvements have been made in challenge models, reducing incubation times to better simulate natural infection conditions.

• Autovaccines: As an alternative, autovaccines or autogenous bacterins have been developed and implemented. However, there are significant knowledge gaps regarding the efficacy of these biological products and the host defense mechanisms.

Research is moving toward new vaccine technologies, including the use of recombinant proteins, mRNA vaccines, and the use of outer membrane vesicles (OMVs) as potential vaccines. OMVs from T. maritimum have been shown to play a role in adhesion, biofilm formation, and the secretion of lytic enzymes. The combination of OMVs with other antigens could be a promising strategy.

On the other hand, conventional vaccines may not be effective against all strains or serotypes of T. maritimum. Therefore, identifying the protective antigens and developing multivalent or broad-spectrum vaccines is crucial.

Furthermore, some vaccination trials in salmonids have shown little or no protection, while others have obtained more promising results with adjuvant-based vaccines. This highlights the complexity of the interaction between the vaccine, host, and pathogen.

The development of vaccines against T. maritimum is challenging due to strain diversity, the lack of reliable challenge models, the host immune response, and the complexity of the bacterium’s pathogenesis. Although a vaccine is available for turbot, new strategies are needed to protect other fish species. Romero (2023) reported the development of the 23010 vaccine, based on a T. finnmarkense isolate, which is effective in protecting rainbow trout against tenacibaculosis, and cross-species reactivity suggests the potential for a vaccine to provide protection against multiple Tenacibaculum species.

Research is focusing on identifying protective antigens, improving vaccine technologies, optimizing adjuvants, and developing autovaccines. The use of OMVs and the creation of multivalent vaccines are promising approaches in this field. Ongoing research and collaboration are essential to finding effective and sustainable solutions for controlling tenacibaculosis.

Alternative Control Methods

Alternative control methods to antibiotics for combating Tenacibaculum maritimum and tenacibaculosis are being explored due to growing concerns about antimicrobial resistance and its negative effects on fish health and the environment. These methods focus on strengthening the fish’s immune system, preventing infection, and reducing the need for antibiotic treatments.

Probiotics

Some probiotics, such as Nocardiopsis dassonvillei and Roseobacter (Phaeobacter piscinae), have been shown to have antimicrobial activity against T. maritimum. These probiotics can produce substances that inhibit pathogen growth or stimulate the fish’s immune system. Some strains of probiotics isolated from the gastrointestinal tract of flatfish have also shown inhibition against T. maritimum.

Administering probiotics can help maintain a balanced intestinal microbiota, which is crucial for fish health and disease resistance.

Herbal and Natural Compound Treatments

Some research has explored the use of plant extracts and other natural compounds with antimicrobial properties. These compounds could help control the infection without the adverse effects of antibiotics.

Phages

Phage therapy, which uses viruses that infect bacteria to control pathogen growth, is a field of research that is beginning to be explored.

Understanding the Microbiota

Understanding the composition and role of the microbiota in fish health has become a key research area to understand how microbiota can be manipulated to prevent T. maritimum infections.

Further research is needed on how dysbiosis (changes in the microbiota) occurs to reduce pathogen proliferation.

Advances and Challenges in Research

The key scientific advances and persistent challenges related to Tenacibaculum maritimum can be summarized as follows:

Scientific Advances

• Identification and Genetic Characterization: Significant progress has been made in understanding the genetic diversity of T. maritimum. Multilocus sequence analysis (MLSA) and genotyping have allowed the identification of different strains and genetic groups. This is crucial for epidemiological tracking of the bacteria and vaccine development.
• Development of Molecular Diagnostic Methods: PCR-based methods have been developed for the rapid and accurate detection of T. maritimum. Additionally, MALDI-TOF mass spectrometry has been established as an alternative tool for the rapid identification of Tenacibaculum species. These advances allow for early detection of the disease and better outbreak management.
• Genome Characterization: The analysis of the T. maritimum genome has revealed genes related to virulence and pathogenicity, including toxins, enzymes, and secretion systems. Identifying these virulence factors is essential for understanding how the bacteria cause disease and for developing control strategies.
• Understanding the O Antigen Structure: The identification of the O-AGC gene cluster in T. maritimum and the development of multiplex PCR-based serotyping schemes have enabled the differentiation of serotypes and improved understanding of strain variability.

Challenges

• Strain Diversity: The genetic and antigenic diversity among T. maritimum strains remains a significant challenge. This diversity complicates the development of vaccines, diagnostics, and therapeutics that are effective against all strains.
• Species-Specific Response: The immune response to T. maritimum is highly species-specific, which limits the generalization of vaccines developed for one fish species to others.
• Pathogenesis and Virulence Factors: Despite advances in understanding the pathogenicity of T. maritimum, much remains unknown about the exact mechanisms by which it causes disease. Further research is needed to identify all the factors involved in virulence and disease progression.

Conclusion

The treatment and control of T. maritimum require an integrated approach, including the use of antibiotics, environmental management, vaccination, and alternative methods like probiotics and natural compounds. Advances in molecular diagnostics, vaccine development, and understanding the pathogen’s genetic and virulence factors hold promise for better management of tenacibaculosis. However, challenges remain, and further research is essential to improve control strategies and reduce the impact of this disease on aquaculture.

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