Exploring fish microbial communities to mitigate emerging diseases in aquaculture

FEMS Microbiology Ecology, 94, 2018, fix161 doi: 10.1093/femsec/fix161 Advance Access Publication Date: 29 November 2017 Minireview MINIREVIEW Irene de Bruijn1,† , Yiying Liu1,∗,† , Geert F. Wiegertjes2 and Jos M Raaijmakers1,3 1 Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Droevendaalsesteeg 10, Wageningen 6708PB, The Netherlands, 2 Cell Biology and Immunology group, Department of Animal Sciences, Wageningen University & Research, De Elst 1, Wageningen 6708WD, The Netherlands and 3 Institute of Biology (IBL), Leiden University, Sylviusweg 72, Leiden 2333 BE, Leiden, The Netherlands ∗ Corresponding author: I. de Bruijn, Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), 6708PB Wageningen, The Netherlands. Tel: 0031 317 473496; E-mail: † Shared first authors. One sentence summary: This review describes insights in the diversity and functions of the fish bacterial communities elucidated with next-generation sequencing and discusses the potential of the microbes to mitigate (re-)emerging diseases in aquaculture. Editor: Marcus Horn ABSTRACT Aquaculture is the fastest growing animal food sector worldwide and expected to further increase to feed the growing human population. However, existing and (re-)emerging diseases are hampering fish and shellfish cultivation and yield. For many diseases, vaccination protocols are not in place and the excessive use of antibiotics and other chemicals is of substantial concern. A more sustainable disease control strategy to protect fish and shellfish from (re-)emerging diseases could be achieved by introduction or augmentation of beneficial microbes. To establish and maintain a ‘healthy’ fish microbiome, a fundamental understanding of the diversity and temporal-spatial dynamics of fish-associated microbial communities and their impact on growth and health of their aquatic hosts is required. This review describes insights in the diversity and functions of the fish bacterial communities elucidated with next-generation sequencing and discusses the potential of the microbes to mitigate (re-)emerging diseases in aquaculture. Keywords: aquaculture; fish; emerging diseases; microbiomes; beneficial microbes INTRODUCTION The United Nations Food and Agricultural Organization (FAO) predicts that the world’s food and feed supply needs to grow by 70% to support the growing human population by 2050. Currently, aquaculture is the fastest growing animal food sector worldwide (FAO 2014). However, fish and shellfish production is limited by several emerging diseases caused by viruses, bacteria, fungi, oomycetes, amoebas and other ectoparasites. Bacterial fish diseases are typically addressed by antibiotics (Romero et al. 2012; Cabello et al. 2013), viral diseases by vaccination (Evensen and Leong 2013) and parasitic diseases by chemical treatment (Burridge et al. 2010). However, the risk of antibiotic resistance development and the transfer of antibiotic resistance genes to other animal pathogens, as well as concerns for environmental impact and consumer safety, have stimulated the need for new sustainable control measures (Brandt et al. 2015). Vaccination is a sustainable control measure, but various viral and bacterial fish diseases, and more specifically fungal and oomycete diseases, cannot yet be controlled by vaccination (Evensen and Received: 12 May 2017; Accepted: 28 November 2017  C FEMS 2017. All rights reserved. For permissions, please e-mail: 1 Exploring fish microbial communities to mitigate emerging diseases in aquaculture 2 FEMS Microbiology Ecology, 2018, Vol. 94, No. 1 MICROBIOMES In this review, the microbiome is defined as described by Joshua Lederberg: ‘the totality of microbes, their genomes and their interactions in a particular environment’. There is increasing evidence that microbial consortia rather than single microbial species are associated with health and disease (Gilbert et al. 2016). The impact of microbial consortia on early development and health of their eukaryotic hosts is gaining increased attention, with new ‘omics’-based technologies allowing for in-depth characterizations of microbial communities and functions in diverse ecosystems. Indeed, constituents within the human gut microbiomes can significantly drive or suppress disease development (Round, O’Connell and Mazmanian 2010; Everard et al. 2013; Gilbert et al. 2016), whereas environmental changes or infections can substantially influence the human gut microbiome by causing blooms of microbes that otherwise are present at low abundance (Stecher, Maier and Hardt 2013). In terrestrial farmed animals, sudden changes like the use of antibiotics or dietary changes can cause substantial shifts in the gut microbial composition leading to disease susceptibility (Gresse et al. 2017, Cisek and Binek 2014; Fecteau et al. 2016; Fouhse, Zijlstra and Willing 2016). Similar observations have been made for the gut of insects, whose microbiomes can influence insect development by increasing nutrient uptake and stimulating immunity maturation (Weiss and Aksoy 2011). Also for plants, microbiota play an important role in the protection against biotic and abiotic stress factors (Berendsen, Pieterse and Bakker 2012; Vorholt 2012; Bul- garelli et al. 2013; Philippot et al. 2013; Turner et al. 2013; Mendes and Raaijmakers 2015). In line with these findings, microbial communities of fish may harbor substantial potential to modulate health and disease. Due to the complex structure of microbial communities, disentangling interactions and identifying keystone species for specific functions is enormously challenging, especially when environmental influences on population dynamics and activities are taken into account. Microbiome research of humans and other eukaryotes typically describes correlations between microbiome composition and diseases, but it remains a challenge which taxonomic or functional changes in the microbiome are actually causal for disease development or disease protection (Gilbert et al. 2016; Raaijmakers and Mazzola 2016). Hence, a systems-based understanding of the dynamics and functions of microbial communities for their fish and shellfish hosts is needed to enable a more profound selection of beneficial (micro)organisms for augmentation of microbial communities to achieve more sustainable disease control strategies in aquaculture. This review describes the current state-of-the-art of fish microbial community research using next generation sequencing and provides an outlook into the functional potential of fish-associated microbes to control (re-) emerging diseases in aquaculture. Diversity of fish microbiota Traditionally, microbes associated with aquatic animals and their environment have been isolated on general and selective agar media. Since only a proportion of the viable microbes in various aquatic environments are culturable (Amann, Ludwig and Schleifer 1995), culture-independent met (...truncated)