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The microbiome of deep-sea fish reveals new microbial species and a sparsity of antibiotic resistance genes.

ABSTRACT: Adaptation to life in the deep-sea can be dramatic, with fish displaying behaviors and appearances unlike those seen in any other aquatic habitat. However, the extent of which adaptations may have developed at a microbial scale is not as clear. Shotgun metagenomic sequencing of the intestinal microbiome of 32 species of deep-sea fish from across the Atlantic Ocean revealed that many of the associated microbes differ extensively from those previously identified in reference databases. 111 individual metagenome-assembled genomes (MAGs) were constructed representing individual microbial species from the microbiomes of these fish, many of which are potentially novel bacterial taxa and provide a window into the microbial diversity in this underexplored environment. These MAGs also demonstrate how these microbes have adapted to deep-sea life by encoding a greater capacity for several cellular processes such as protein folding and DNA replication that can be inhibited by high pressure. Another intriguing feature was the almost complete lack of genes responsible for acquired resistance to known antibiotics in many of the samples. This highlights that deep-sea fish microbiomes may represent one of few animal-associated microbiomes with little influence from human activity. The ability of the microbes in these samples to bioluminesce is lower than expected given predictions that this trait has an important role in their life cycle at these depths. The study highlights the uniqueness, complexity and adaptation of microbial communities living in one of the largest and harshest environments on Earth.

SUBMITTER: Collins FWJ

PROVIDER: S-EPMC8115496 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Aquaculture is a fast-growing animal food sector, and freshwater fish farming is particularly common in Central and Eastern Europe. As the biodiversity of fishery ponds is changed toward fulfilling the industrial needs, precautions should be taken to keep the system sustainable and protect the adjacent environment from possible damage. Due to risk of infectious diseases, antibiotics are used in aquaculture production systems. The constant exposure to antimicrobials can contribute to the rise of antibiotic resistance in aquaculture products and the adjacent ecosystems, with possibility of dissemination to the wider environment as well as between animals and humans. Even though previous studies have found antibiotic resistance genes in the sediments and water of farming ponds, the tendency and direction of spreading is not clear yet. The objective of this project was to evaluate the influence of intensive fish farming on the condition of water bodies used for the aquaculture and the environment, concentrating on the impact of the aquaculture on the surrounding water ecosystems as well as the possibility of transferring the pollutants and antibiotic resistance genes to both environment and the human hosts. Combined measurement of antibiotic and heavy metal contamination, toxicity assessment, microorganism diversity, and the detection of common antibiotic resistance genes was performed in the sediments of one fishery farm ponds as well as sampling points upstream and downstream. All the tested sediment samples did not show significantly elevated heavy metal concentrations and no substantial veterinary antibiotic pollution. From the antibiotic resistance genes tested, the presence of aminoglycoside and β-lactam resistance determinants as well as the presence of integrons could be of concern for the possibility of transfer to humans. However, despite the lack of heavy metal and antibiotic pollution, the sediments showed toxicity, the cause of which should be explored more.

Project description:Our previous studies showed that particular antibiotic resistance genes (ARGs) were enriched locally in sediments below fish farms in the Northern Baltic Sea, Finland, even when the selection pressure from antibiotics was negligible. We assumed that a constant influx of farmed fish feces could be the plausible source of the ARGs enriched in the farm sediments. In the present study, we analyzed the composition of the antibiotic resistome from the intestinal contents of 20 fish from the Baltic Sea farms. We used a high-throughput method, WaferGen qPCR array with 364 primer sets to detect and quantify ARGs, mobile genetic elements (MGE), and the 16S rRNA gene. Despite a considerably wide selection of qPCR primer sets, only 28 genes were detected in the intestinal contents. The detected genes were ARGs encoding resistance to sulfonamide (sul1), trimethoprim (dfrA1), tetracycline [tet(32), tetM, tetO, tetW], aminoglycoside (aadA1, aadA2), chloramphenicol (catA1), and efflux-pumps resistance genes (emrB, matA, mefA, msrA). The detected genes also included class 1 integron-associated genes (intI1, qacEΔ1) and transposases (tnpA). Importantly, most of the detected genes were the same genes enriched in the farm sediments. This preliminary study suggests that feces from farmed fish contribute to the ARG enrichment in farm sediments despite the lack of contemporaneous antibiotic treatments at the farms. We observed that the intestinal contents of individual farmed fish had their own resistome compositions. Our result also showed that the total relative abundances of transposases and tet genes were significantly correlated (p = 0.001, R2 = 0.71). In addition, we analyzed the mucosal skin and gill filament resistomes of the farmed fish but only one multidrug-efflux resistance gene (emrB) was detected. To our knowledge, this is the first study reporting the resistome of farmed fish using a culture-independent method. Determining the possible sources of ARGs, especially mobilized ARGs, is essential for controlling the occurrence and spread of ARGs at fish farming facilities and for lowering the risk of ARG spread from the farms to surrounding environments.

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The microbiome of deep-sea fish reveals new microbial species and a sparsity of antibiotic resistance genes.

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