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The Roseobacter-Group Bacterium Phaeobacter As Safe Probiotic Solution for Aquaculture

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The Roseobacter-Group Bacterium Phaeobacter As Safe Probiotic Solution for Aquaculture Downloaded from orbit.dtu.dk on: Oct 02, 2021 The Roseobacter-group bacterium Phaeobacter as safe probiotic solution for aquaculture Sonnenschein, Eva C.; Jimenez, Guillermo; Castex, Mathieu; Gram, Lone Published in: Applied and Environmental Microbiology Link to article, DOI: 10.1128/AEM.02581-20 Publication date: 2021 Document Version Peer reviewed version Link back to DTU Orbit Citation (APA): Sonnenschein, E. C., Jimenez, G., Castex, M., & Gram, L. (2021). The Roseobacter-group bacterium Phaeobacter as safe probiotic solution for aquaculture. Applied and Environmental Microbiology, 87(5), [e02581- 20]. https://doi.org/10.1128/AEM.02581-20 General rights Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. Users may download and print one copy of any publication from the public portal for the purpose of private study or research. You may not further distribute the material or use it for any profit-making activity or commercial gain You may freely distribute the URL identifying the publication in the public portal If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. 1 The Roseobacter-group bacterium Phaeobacter as safe probiotic solution for aquaculture 2 Eva C. Sonnenschein1*, Guillermo Jimenez2, Mathieu Castex2, Lone Gram1 3 1 Department of Biotechnology and Biomedicine, Technical University of Denmark, Søltofts 4 Plads Bldg. 221, 2800 Kgs. Lyngby, Denmark. 5 2 Lallemand SAS, Blagnac Cedex, France. 6 * corresponding author e-mail: [email protected] 7 Abstract 8 Phaeobacter inhibens has been assessed as a probiotic bacterium for application in aquaculture. 9 Studies addressing the efficacy and safety indicate that P. inhibens maintains it antagonistic 10 activity against pathogenic vibrios in aquaculture live cultures (live feed and fish egg/larvae), 11 while having no or a positive effect on the host organisms, and a minor impact on the host 12 microbiomes. While producing antibacterial and algicidal compounds, no study has so far found 13 a virulent phenotype of P. inhibens cells against higher organisms. Additionally, an in silico 14 search for antibiotic resistance genes using published genomes of representative strains did not 15 raise concern regarding the risk for antimicrobial resistance. P. inhibens occurs naturally in 16 aquaculture systems supporting its safe usage in this environment. Concluding, at the current 17 state of knowledge, P. inhibens is a “safe-to-use” organism. 18 19 INTRODUCTION 20 Phaeobacter inhibens is a marine alphaproteobacterium with potential for application as a 21 probiotic bacterium in marine aquaculture systems. P. inhibens is a representative of the 22 Roseobacter group that is widespread and an environmentally important marine group of 1 23 bacteria. P. inhibens serves as a heterotrophic marine model organism to understand fundamental 24 processes such as adaptation to an attached lifestyle and interactions with higher organisms (1). 25 Its probiotic activity against fish pathogenic bacteria is primarily due to the production of the 26 antibacterial compound tropodithietic acid (TDA) (2). TDA is bacteriocidal to both fish and 27 human bacterial pathogens. The applicability of P. inhibens as a probiotic bacterium in marine 28 aquaculture has been assessed in several studies and has recently been compared to that of other 29 probiotics (3). The bacterium is naturally present in aquaculture systems and it is able to inhibit 30 fish pathogenic bacteria. Most studies have been performed on its activity against economically 31 important Vibrio spp. such as V. anguillarum and V. vulnificus, but it also inhibits other fish 32 pathogens such as Aeromonas and Tenacibaculum spp. (4–7). This is seen both in laboratory 33 based agar-assays, and in live feed used in marine larval rearing. The ability to inhibit fish 34 pathogenic Vibrio has been demonstrated in both axenic and non-axenic live feed systems (6, 8– 35 11). Also, in model challenge trials, P. inhibens can decrease the mortality of fish larvae 36 challenged with pathogenic Vibrio (10). 37 Farming of fish and shellfish is of great importance to supply protein for food and feed for the 38 growing world population. Catches from wild fish have stagnated (or even declined) since the 39 mid 1980s and the increase in fish production comes almost exclusively from aquaculture (12). In 40 intense animal rearing systems, infectious agents such as pathogenic bacteria spread rapidly and 41 one particularly sensitive stage is the larval development. Fish larvae do not have a developed 42 immune system and vaccination can therefore not be used as disease preventive measure (13). 43 During larval rearing, opportunistic and pathogenic bacteria are easily introduced via live feed 44 and infections can spread rapidly, eradicating the complete larval batch (14). Antibiotics have 45 been used to control these infections, however due to the risk of bacteria developing and 46 spreading antibiotic resistance, other measures must be found. One strategy for limiting the 2 47 proliferation of bacterial pathogens in live feed and fish larvae is the use of probiotic bacteria 48 (15). Probiotic microorganisms have been defined by FAO and WHO (16) as “live 49 microorganisms which when administered in adequate amounts confer a health benefit on the 50 host”. This approach presents an environmentally sustainable and economically viable solution to 51 counteract the economic loss caused by bacterial pathogens in aquaculture systems. 52 53 P. inhibens has been shown to antagonize many fish pathogenic bacteria such as Vibrio spp. (6, 54 7). In the laboratory, resistance to the effector molecule, TDA, could not be selected for in 55 pathogenic bacteria, likely because the molecule as an antiporter destabilizes the bacterial proton 56 motive force (17, 18). Interestingly, despite this broad range effect, addition of the bacterium to 57 live feed only causes minor changes in the microbiome of the live feed (19). A search in the 58 whole genome sequence of P. inhibens DSM 17395 for the presence of known antimicrobial 59 resistance (AMR) genes to antimicrobials relevant to their use in humans and animals was 60 performed, as indicated in the European Food Safety Authority (EFSA) Guidance on the 61 characterization of microorganisms used as feed additives or as production organisms (EFSA, 62 2018). For this purpose, a comparison against up-to-date databases (e.g. ARG-ANNOT, CARD 63 and ResFinder) was performed. This article provides an overview of the genetics and physiology 64 of P. inhibens and summarizes the current information on the safety of P. inhibens for its use as a 65 probiotic in aquaculture. 66 67 TAXONOMIC CLASSIFICATION, PHENOTYPE AND GENETIC DIVERSITY OF P. 68 INHIBENS 69 The obligate marine genus Phaeobacter belongs to the Roseobacter group, the marine subgroup 70 within the family Rhodobacteraceae (20). Due to the ease at which Rhodobacteraceae can be 3 71 cultured and the prevalence of this family in marine ecosystems, today, 181 different genera have 72 been reported (according to NCBI taxonomy); however, over the recent years, there has also been 73 several drastic reclassifications at genus and species level (21, 22). Currently, the Phaeobacter 74 genus comprises six species: P. gallaeciencis (21), P. inhibens (21), P. marinintestinus (23), P. 75 piscinae (24), P. porticola (25), and P. italicus (26) (Fig. 1). However the phylogenetic diversity 76 within the genus is low (22) and species level distinction based on 16S rRNA gene sequences is 77 difficult (27). In particular, differentiating between P. inhibens, P. gallaeciensis and P. piscinae 78 is challenging (24). When comparing the whole nucleotide data per genome using the average 79 nucleotide identity, P. piscinae (89.7%) and P. gallaeciensis (89.3%) are closest related to P. 80 inhibens (Fig. 1). P. porticola (84.5%) and P. italicus (78.6%) are less similar to P. inhibens. 81 82 The species Phaeobacter inhibens with the type strain DSM 16374T (also named LMG 22475T or 83 T5T) was described in 2006 as a reclassification of the species Roseobacter gallaeciensis (21). 84 Additional well-characterized strains include DSM 17395 (initially isolated as type strain of P. 85 gallaeciensis BS107; (28, 29)) and 2.10 (also named DSM 24588) (30). The strain DSM 17395 86 was considered identical with the strain CIP 105210 as both represented culture collection 87 deposits of the P. gallaeciensis type strain BS107T; however, further genomic analysis revealed 88 that DSM 17395 is more closely affiliated to P. inhibens T5T and represents a strain distinct from 89 CIP 105210 (29). CIP 105210T (= DSM 26640T = BS107T) is now the type strain of P. 90 gallaeciensis. In many studies, the descriptions of the source of strain BS107T is unclear and 91 accordingly, the biological identity of the strain described in these studies remains unknown. 92 93 Extensive physiological data on P. inhibens are available (21). P. inhibens clearly differentiates 94 morphologically from other marine bacteria due to the formation of brown colonies on nutrient 4 95 rich iron-containing medium due to precipitation of a brown TDA-iron complex (31). In liquid 96 medium, cells are motile, but tend to form star-shaped aggregates, also called rosettes (32). Based 97 on the currently available 22 genomes (Table 1), genomes of P. inhibens strains have an average 98 size of 4.36 Mb (4.02 – 4.84 Mb) and an average GC content of 59.8% (59.5 – 60.0%). The 99 nucleotide information is structured in one chromosome and several plasmids (3 to 10 plasmids) 100 including few very large (up to 262 kb) plasmids, or chromids. The genomes encode on average 101 4128 genes (3771 – 4609 genes).
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