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First Genome of Labyrinthula, an Opportunistic Seagrass Pathogen, Reveals Novel Insight

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First Genome of Labyrinthula, an Opportunistic Seagrass Pathogen, Reveals Novel Insight bioRxiv preprint doi: https://doi.org/10.1101/2020.09.14.297390; this version posted September 15, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 First genome of Labyrinthula, an opportunistic seagrass pathogen, reveals novel insight 2 into marine protist phylogeny, ecology and CAZyme cell-wall degradation 3 Mun Hua Tan1,2,3,4, Stella Loke1,2, Laurence J. Croft1,2, Frank H. Gleason5, Lene Lange6, Bo 4 Pilgaard7, Stacey M. Trevathan-Tackett1* 5 6 1Centre of Integrative Ecology, School of Life and Environmental Sciences Deakin 7 University, Geelong, Australia 8 2Deakin Genomics Centre, Deakin University, Geelong, Australia 9 3School of BioSciences, Bio21 Institute, University of Melbourne, Australia 10 4Department of Microbiology and Immunology, University of Melbourne, Bio21 Institute, 11 Melbourne, Australia 12 5School of Life and Environmental Sciences, University of Sydney, Sydney, 2006, New 13 South Wales, Australia 14 6BioEconomy, Research & Advisory, Valby, 2500 Copenhagen, Denmark 15 7Protein Chemistry and Enzyme Technology, Department of Bioengineering, Technical 16 University of Denmark, Kgs. Lyngby, Denmark 17 18 19 * Corresponding Author: Dr Stacey Trevathan-Tackett, [email protected], 20 Deakin University, 221 Burwood Hwy, Burwood, Victoria, Australia 3125 21 22 Keywords: evolution; ion regulation; mitochondrial genome; saprobe; Stramenopiles; 23 virulence 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.09.14.297390; this version posted September 15, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 24 Abstract 25 Labyrinthula spp. are saprobic, marine protists that also act as opportunistic pathogens and 26 are the causative agents of seagrass wasting disease (SWD). Despite the threat of local- and 27 large-scale SWD outbreaks, there are currently gaps in our understanding of the drivers of 28 SWD, particularly surrounding Labyrinthula virulence and ecology. Given these 29 uncertainties, we investigated Labyrinthula from a novel genomic perspective by presenting 30 the first draft genome and predicted proteome of a pathogenic isolate of Labyrinthula 31 SR_Ha_C, generated from a hybrid assembly of Nanopore and Illumina sequences. 32 Phylogenetic and cross-phyla comparisons revealed insights into the evolutionary history of 33 Stramenopiles. Genome annotation showed evidence of glideosome-type machinery and an 34 apicoplast protein typically found in protist pathogens and parasites. Proteins involved in 35 Labyrinthula’s actin-myosin mode of transport, as well as carbohydrate degradation were 36 also prevalent. Further, CAZyme functional predictions revealed a repertoire of enzymes 37 involved in breakdown of cell-wall and carbohydrate storage compounds common to 38 seagrasses. The relatively low number of CAZymes annotated from the genome of 39 Labyrinthula SR_Ha_C compared to other Labyrinthulea species may reflect the 40 conservative annotation parameters, a specialised substrate affinity and the scarcity of 41 characterised protist enzymes. Inherently, there is high probability for finding both unique 42 and novel enzymes from Labyrinthula spp. This study provides resources for further 43 exploration of Labyrinthula ecology and evolution, and will hopefully be the catalyst for new 44 hypothesis-driven SWD research revealing more details of molecular interactions between 45 Labyrinthula species and its host substrate. 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.09.14.297390; this version posted September 15, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 46 Introduction 47 Sequencing capabilities of both short and long read technologies have shown marked 48 progress in recent years, resulting in the generation of a large number of contiguous and high 49 quality genome assemblies reported for a myriad of living organisms at an unprecedented 50 pace. As a result of genome sequencing projects at local-to-global scales, we are better 51 resolving linages across the Tree of Life (Lewin et al. 2018), revealing new diversity for 52 underrepresented or unculturable microorganisms (e.g. aquatic and marine protists and 53 zoosporic fungi; Sibbald and Archibald 2017, Lange et al. 2019a) and informing the 54 ecological and functional roles of organisms in the environment (Kyrpides et al. 2014). In 55 marine ecosystems, genomic and transcriptomic sequencing is producing vital information on 56 the ecological roles microorganisms play. For example, genomes of putative pathogens are 57 revealing genes involved in virulence and attachment to the host, as well as mechanisms 58 involved in degrading the host substrate and switching between non-pathogenic and 59 pathogenic lifestyles (Fernandes et al. 2011). These new insights are especially important as 60 marine emergent diseases and opportunistic pathogens are predicted to increase globally in 61 the coming decades due to the suboptimal living conditions for marine biota caused by 62 human- and climate-induced changes (Harvell et al. 1999). 63 64 Seagrass meadows are one such marine ecosystem susceptible to a decline in health and 65 increased infection, as they are subjected to dynamic pressures at the land-sea interface, such 66 as elevated temperatures in shallow regions and run-off-associated turbidity, eutrophication 67 and hyposalinity conditions (Sullivan et al. 2018). There are currently four pathogens that 68 cause disease to multiple seagrass genera: Labyrinthula, Phytophthora, Halophytophthora, 69 and Phytomyxea (Sullivan et al. 2018). Labyrinthula, a heterotrophic, halophytic protist in 70 the Stramenopile lineage, is the causative agent of seagrass wasting disease (SWD). To-date, 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.09.14.297390; this version posted September 15, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 71 it is also the most well-studied seagrass pathogen after being discovered in the early twentieth 72 century when it decimated 90% of the North Atlantic population of the seagrass Zostera 73 marina (Sullivan et al. 2018). Labyrinthula isolates from seagrass leaves have shown variable 74 levels of virulence through laboratory infection trials and associated phylogenetic analyses 75 (Martin et al. 2016, Brakel et al. 2017). Virulent isolates are able to invade the leaf cells of 76 living plants and subsequently cause black leaf lesions, the diagnostic trait of SWD (Sullivan 77 et al. 2018). However, Labyrinthula, is also a ubiquitous commensal saprobe that 78 decomposes marine plants and algae litter, with one species parasitic to turfgrass (Martin et 79 al. 2016). Because of the flexibility of its ecological function, Labyrinthula spp. are 80 considered opportunistic pathogens that in some cases utilise a mild parasitism strategy 81 (Brakel et al. 2017). 82 83 Since its discovery, the advances in our understanding of Labyrinthula species include 84 phylogenetic reclassifications of Labyrinthula (Leander and Porter 2001) and molecular 85 techniques that facilitate detection of Labyrinthula without the need for culturing (Duffin et 86 al. 2020, Lohan et al. 2020). Despite this progress, we still do not completely understand the 87 pathosystem of SWD. For example, it is still under debate whether the conditions that 88 promote SWD rely more on seagrass health and defence capabilities or the virulence and 89 enzymatic capabilities of Labyrinthula isolates and haplotypes, or a combination of host and 90 pathogen characteristics (Martin et al. 2016, Duffin et al. 2020). Much of the new knowledge 91 on the pathosystem has come from the immune and stress response of the seagrass using 92 genomic markers or assays (Brakel et al. 2014, Duffin et al. 2020), as opposed to pathogen 93 virulence (Martin et al. 2016). Furthermore, despite our molecular advances, we also know 94 little about the role of specific organelles, such as the bothrosome, in the hunt and 95 consumption of food sources (Collier and Rest 2019). Next-generation sequencing 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.09.14.297390; this version posted September 15, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 96 technologies are helping us produce new hypotheses for Labyrinthula and SWD. For 97 example, Lohan et al. (2020) questioned how the variation in Labyrinthula diversity links 98 with intra-species diversity of the seagrass host. 99 100 This set of ecological uncertainties constitutes the basis for our interest in sequencing the 101 genome of a Labyrinthula isolate. So far the genomes of only three different genera of the 102 Labyrinthulea class have been
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