Endosymbionts escape dead hydrothermal vent tubeworms to enrich the free-living population.
Theory predicts that horizontal acquisition of symbionts by plants and animals must be coupled to release and limited dispersal of symbionts for intergenerational persistence of mutualisms. For deep-sea hydrothermal vent tubeworms (Vestimentifera, Siboglinidae), it has been demonstrated that a few symbiotic bacteria infect aposymbiotic host larvae and grow in a newly formed organ, the trophosome. However, whether viable symbionts can be released to augment environmental populations has been doubtful, because (i) the adult worms lack obvious openings and (ii) the vast majority of symbionts has been regarded as terminally differentiated. Here we show experimentally that symbionts rapidly escape their hosts upon death and recruit to surfaces where they proliferate. Estimating symbiont release from our experiments taken together with well-known tubeworm density ranges, we suggest a few million to 1.5 billion symbionts seeding the environment upon death of a tubeworm clump. In situ observations show that such clumps have rapid turnover, suggesting that release of large numbers of symbionts may ensure effective dispersal to new sites followed by active larval colonization. Moreover, release of symbionts might enable adaptations that evolve within host individuals to spread within host populations and possibly to new environments.
Department of Limnology and Bio-Oceanography, University of Vienna, A-1090 Vienna, Austria;
Julia
J
Klose
Parsons Laboratory for Environmental Science and Engineering, Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139;
Martin F
MF
Polz
Department of Microbiology and Ecosystem Science, University of Vienna, A-1090 Vienna, Austria;
Michael
M
Wagner
Department of Limnology and Bio-Oceanography, University of Vienna, A-1090 Vienna, Austria; Max Planck Institute for Marine Microbiology, 28359 Bremen, Germany;
Mario P
MP
Schimak
Department of Limnology and Bio-Oceanography, University of Vienna, A-1090 Vienna, Austria; Department of Ecosystem Studies, Royal Netherlands Institute for Sea Research (NIOZ), 4401 NT Yerseke, The Netherlands; German Center for Marine Biodiversity Research, Senckenberg am Meer, 26382 Wilhelmshaven, Germany.
Sabine
S
Gollner
Department of Limnology and Bio-Oceanography, University of Vienna, A-1090 Vienna, Austria; monika.bright@univie.ac.at.
Monika
M
Bright
D000818:Animals; D001419:Bacteria / Q000235:genetics / Q000254:growth & development* / Q000648:ultrastructure; D058491:Bacterial Load; D016923:Cell Death; D004783:Environmental Microbiology; D054884:Host-Pathogen Interactions; D060086:Hydrothermal Vents / Q000469:parasitology*; D017404:In Situ Hybridization, Fluorescence; D007814:Larva / Q000382:microbiology; D046529:Microscopy, Electron, Transmission; D011077:Polychaeta / Q000235:genetics / Q000382:microbiology* / Q000648:ultrastructure; D012336:RNA, Ribosomal, 16S / Q000235:genetics; D012623:Seawater / Q000382:microbiology; D013559:Symbiosis
D012336:RNA, Ribosomal, 16S
Vestimentifera; mutualism stability; symbiont seeding; symbiosis; tubeworms