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Host-Microbe Symbiosis in the Marine Sponge Halichondria Panicea

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Host-Microbe Symbiosis in the Marine Sponge Halichondria Panicea Host-microbe symbiosis in the marine sponge Halichondria panicea Stephen Knobloch Faculty of Life and Environmental Sciences University of Iceland 2019 Host-microbe symbiosis in the marine sponge Halichondria panicea Stephen Knobloch Dissertation submitted in partial fulfilment of a Philosophiae Doctor degree in Biology PhD Committee Viggó Þór Marteinsson Ragnar Jóhannsson Eva Benediktsdóttir Opponents Detmer Sipkema Ólafur Sigmar Andrésson Faculty of Life and Environmental Sciences School of Engineering and Natural Sciences University of Iceland Reykjavik, May 2019 Host-microbe symbiosis in the marine sponge Halichondria panicea Bacterial symbiosis in H. panicea Dissertation submitted in partial fulfilment of a Philosophiae Doctor degree in Biology Copyright © 2019 Stephen Knobloch All rights reserved Faculty of Life and Environmental Sciences School of Engineering and Natural Sciences University of Iceland Askja, Sturlugata 7 101, Reykjavik Iceland Telephone: +354 525 4000 Bibliographic information: Stephen Knobloch, 2019, Host-microbe symbiosis in the marine sponge Halichondria panicea, PhD dissertation, Faculty of Life and Environmental Sciences, University of Iceland, 204 pp. ISBN: 978-9935-9438-8-0 Author ORCID: 0000-0002-0930-8592 Printing: Háskólaprent Reykjavik, Iceland, May 2019 Abstract Sponges (phylum Porifera) are considered one of the oldest extant lineages of the animal kingdom. Their close association with microorganism makes them suitable for studying early animal-microbe symbiosis and expanding our understanding of host-microbe interactions through conserved mechanisms. Moreover, many sponges and sponge- associated microorganisms produce bioactive compounds, making them highly relevant for the biotechnology and pharmaceutical industry. So far, however, it has not been possible to grow biotechnologically relevant sponge species or isolate their obligate microbial symbionts for these purposes. The marine sponge Halichondria panicea inhabits coastal areas worldwide, which makes the sponge easily accessible, and has therefore been a widely studied sponge species in terms of its biology and ecophysiology. However, the stability of its associated microbial community and the functional role of its permanent members has so far remained elusive. Despite previous studies showing bioactive properties of H. panicea, it is yet unknown if these are produced by the sponge itself or by microorganisms found in its body. In this study, the microbial diversity of H. panicea from Icelandic waters was analysed through marker gene sequencing, genomics and bacterial cultivation. We showed that H. panicea from Icelandic water hosts a dominant bacterial symbiont across geographical locations and seasons whereas other bacteria are geographically and temporally transient. Functional genomic analysis of the dominant symbiont, for which we propose a candidate status with the name “Candidatus Halichondribacter symbioticus”, showed a lack of regulatory genes in line with its obligate symbiotic lifestyle. In addition, it is enriched in sponge symbiont specific gene families related to host-symbiont interactions and defence. Despite the presence of a putative bacteriocin gene cluster, “Ca. H. symbioticus” does not appear to be the source of other bioactive secondary metabolites in this sponge. A comparison of different methods for ex situ cultivation of H. panicea showed that, while different cultivation set-ups allowed for successful maintenance of the sponge itself, only certain conditions also maintained “Ca. H. symbioticus” at a high relative abundance in the sponge body. Based on these results a novel method for sponge-microbe co-cultivation was demonstrated which increases the enriched bacterial diversity compared to standard plating methods. Although “Ca. H. symbioticus” remains un-isolated, other selected isolated bacteria from H. panicea were subjected to antimicrobial activity assays, genome sequencing and strain characterisation leading to the description of two novel species of marine bacteria and one novel putative host-associated bacterium. Due to the presence of a dominant bacterial symbiont and the amenability of H. panicea towards laboratory cultivation, the H. panicea – “Ca. H. symbioticus” system represents a promising model for studying early animal-microbe symbiosis. The results from this study lay the ground work for future studies exploring the interactions between H. panicea and “Ca. H. symbioticus”. Útdráttur Svampar (phylum Porifera) er talin ein af elstu núlifandi fylkingum dýraríkisins. Náin tengsl þeirra við örverur gera þá áhugaverða og heppilega til rannsókna á fyrstu gerðum samlífis dýra og örvera og til að auka almennt skilning okkar á þessu varðveitta samspili og virkni þess. Að auki framleiða margir svampar og samlífisörverur þeirra lífvirk efnasambönd sem gera þá áhugaverða fyrir líftækni- og lyfjaiðnaðinn. Ekki hefur enn tekist að rækta upp svampa fyrir líftækni eða lyfjaiðnaðinn eða einangra skilyrtar samlíförverur þeirra í þeim tilgangi. Sjávarsvampurinn Halichondria panicea (Brauðsvampur) finnst á strandsvæðum víða um heim. Hann er því aðgengilegur og hefur líffræði hans og vistlífeðlisfræði verið rannsökuð töluvert. Hins vegar er lítið vitað um sambýlisörveruflóru hans og hlutverk hennar í samlífinu. Þrátt fyrir að fyrri rannsóknir hafi sýnt fram á lífvirkni efna sem einangruð voru úr H. panicea, er enn ekki vitað hvort þau eru framleidd af svampinum sjálfum eða samlífisörverum hans. Í þessari rannsókn var fjölbreytileiki örvera H. panicea svamps, sem tekin var úr íslensku sjávarumhverfi, skoðaður með merkigenaraðgreiningu, auk raðgreiningu genamengja (metagenom) og erfðamengja ræktaðra baktería. Við sýnum fram á að H. Panicea, úr íslensku umhverfi, hýsir eina ríkjandi bakteríutegund. Tegundin sem fékk heitið “Candidatus Halicondribacter symbioticus”, er einnig til staðar í öðrum H. panicea svömpunum sem rannsakaðir hafa verið frá mismunandi stöðum og óháð árstíðum. Hins vegar eru aðrar sambýlisörverur óskilyrtar og meira bundnar við stað og tíma. Greining á genamengi ríkjandi skilyrtu bakteríunnar sýnir fram á að algeng stýrigen vantar í erfðamengi bakteríunnar. Það er í samræmi við hið skilyrta samlífsform en skortur á stýrigenum algengur í ákveðnum genafjölskyldum tengdum samlífisforminu og vörnum þess. Þrátt fyrir að genaklasi fyrir smíði á lífvirka efninu bacteriocin sé til staðar í “Candidatus Halichondribacter symbioticus” virðist sem það komi ekki við sögu við framleiðslu lífvirkra efna eða „secondary metabolites”. Bornar voru saman mismunandi aðferðir við ræktun (ex situ) á H. panicea og sýnt fram á að þó að mismunandi uppsetning búnaðar viðhéldi svampinum á lífi, þá var eingöngu hægt að viðhalda "Ca. H. symbioticus " í miklu magni í vefjum svampsins við ákveðnar aðstæður. Á grunni þessara niðurstaðna var þróuð ný aðferð við samræktun á svampi og örverum sem auðgar og eykur fjölbreytileika örveranna samanborið við venjulegar ræktunaraðferðir á agar skálum. Þó "Ca. H. symbioticus " sé enn óeinangruð, þá voru aðrar bakteríur einangraðar úr H. panicea og voru valdar bakteríur rannsakaðar með tilliti til framleiðslu lífvirkra efna. Ennfremur var erfðamengi þeirra raðgreint og efnaskipti rannsökuð. Út frá niðurstöðum þessara rannsókna var tveimur nýjum sjávarbakteríutegundum lýst og einni nýrri sambýlistegund. Þar sem sambýlisbakterían er ríkjandi og unnt er að rækta H. panicea í rannsóknarumhverfi er "Ca. H. symbioticus " samrækt heppilegt módel til rannsókna á samspili samlífisörvara og dýra. Niðurstöðurnar úr þessari rannsókn leggja því grunninn að framtíðarrannsóknum á samspili H. panicea og "Ca. H. symbioticus " To Rebecca, Sascha and Nora For all the love, patience and support. Table of Contents List of Figures ..................................................................................................................... xi List of Tables ...................................................................................................................... xii List of Papers .................................................................................................................... xiii List of Published Nucleotide Sequences ......................................................................... xiv Abbreviations ..................................................................................................................... xv Acknowledgements .......................................................................................................... xvii 1 Introduction ..................................................................................................................... 1 1.1 Animal-microbe symbiosis...................................................................................... 1 1.1.1 Definition of symbiosis .................................................................................. 1 1.1.2 Animal-microbe coevolution and interactions ............................................... 1 1.1.3 Model systems ............................................................................................... 3 1.1.4 Metataxonomics and genomics as tools to elucidate animal-microbe relationships ................................................................................................... 5 1.2 Marine sponges and their associated microorganisms ............................................ 6 1.2.1 The phylum Porifera ...................................................................................... 6 1.2.2 Sponge-associated microorganisms
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