Snails associated with the coral-killing sponge Terpios hoshinota in Okinawa Island, Japan

Terpios hoshinota is a thin encrusting sponge that overgrows live scleractinian corals and it is linked to coral loss in many reefs. However, our knowledge of the species associated with this sponge species is poor. During a periodical survey of T. hoshinota in 2020, we found tiny snails crawling on the sponge in the subtropical waters around Okinawa Island, Japan. We observed egg capsules inside the sponge tissue and veliger larvae released from the egg capsules. Molecular analyses of both the snails and veliger larvae (cytochrome oxidase I, COI) showed that they were identical and belonged to Joculator sp. (family Cerithiopsidae). There was no direct observation of predation on the sponge by this snail; however, to the best of our knowledge, this is the first report on a close association between a snail and the sponge T. hoshinota.

Testing of how and why the Terpios hoshinota sponge kills stony corals

An encrusting sponge, Terpios hoshinota, has the potential to infect all species of stony corals in shallow reefs and killing them. It caused a decline in coral coverage in two south-eastern islands of Taiwan. We proposed two hypotheses to examine how the sponges kill the corals, namely, light blocking and toxins, and tested by in-situ experiments. The results revealed that both light blocking, sponge toxins, and particularly the combination of both factors were effective at inducing tissue damage in stony corals over a short period. Second, to answer why the sponges killed the corals, we tested two hypotheses, namely, gaining nutrients versus gaining substrates for the sponge. By analyzing the stable isotopes 13C and 15N, as well as exploiting an enrichment experiment, it was possible to determine that only approximately 9.5% of the carbon and 16.9% of the nitrogen in the newly grown sponge tissues originated from the enriched corals underneath. The analysis also revealed that the control corals without isotope enrichment had higher δ13C and δ15N than the control sponges, which was an additional indication that T. hoshinota did not rely heavily on corals for nutrients. Therefore, our results support the hypothesis that the encrusting sponge did not kill corals for food or nutrients, but rather for the substrate.

Prevalence, complete genome and metabolic potentials of a phylogenetically novel cyanobacterial symbiont in the coral-killing sponge, Terpios hoshinota

Terpios hoshinota is a ferocious, space-competing sponge that kills a variety of stony corals by overgrowth. Outbreaks of this species have led to intense coral reef damage and declines in living corals on the square kilometer scale in many geographical locations. Our large-scale 16S rRNA gene survey across three oceans revealed that the core microbiome of T. hoshinota included operational taxonomic units (OTUs) related to Prochloron, Endozoicomonas, Pseudospirillum, SAR116, Magnetospira, and Ruegeria. A Prochloron- related OTU was the most dominant cyanobacterium in T. hoshinota in the western Pacific Ocean, South China Sea, and Indian Ocean. The complete metagenome-assembled genome of the Prochloron-related cyanobacterium and our pigment analysis revealed that this bacterium had phycobiliproteins and phycobilins and lacked chlorophyll b, inconsistent with the iconic definition of Prochloron. Furthermore, the phylogenetic analyses based on 16S rRNA genes and 120 single-copy genes demonstrated that the bacterium was phylogenetically distinct to Prochloron, strongly suggesting that it should be a sister taxon to Prochloron; we therefore proposed this symbiotic cyanobacterium as a novel species under a new genus: Candidatus Paraprochloron terpiosii. With the recovery of the complete genome, we characterized the metabolic potentials of the novel cyanobacterium in carbon and nitrogen cycling and proposed a model for the interaction between Ca. Pp. terpiosi LD05 and T. hoshinota. In addition, comparative genomics analysis revealed that Ca. Paraprochloron and Prochloron showed distinct features in transporter systems and DNA replication.ImportanceThe finding that one species predominates cyanobacteria in T. hoshinota from different geographic locations indicates that this sponge and Ca. Pp. terpiosi LD05 share a tight relationship. This study builds the foundation for T. hoshinota’s microbiome and paves a way for understanding the ecosystem, invasion mechanism, and causes of outbreak of this coral-killing sponge. Also, the first Prochloron-related complete genome enables us to study this bacterium with molecular approaches in the future and broadens our knowledge of the evolution of symbiotic cyanobacteria.

GROWTH RATE, SPATIAL-TEMPORAL VARIATION AND PREVALENCE OF THE ENCRUSTING CYANOSPONGE (Terpios hoshinota) IN SERIBU ISLANDS, JAKARTA

Terpios hoshinota is a cyanosponge encrusted on the substrate in coral reefs that may cause mass mortality on the infested corals. This research was conducted to investigate the magnitude of damage level of corals due to the T. hoshinota outbreaks by assessing its growth rate, spatiotemporal variation, and prevalence between two sites in Seribu Islands. Four-time observation (T0-T3) in over 18 months (2016-2017) was conducted to see the growth level of sponge using a permanently quadratic photo transect method of 5x5 m (250.000cm2). The total coverage area of sponge on study site in the T0 was 65.252cm2 and becomes 81.066cm2 in T3. The highest level occurred on T2 of 2.051cm2/months in Dapur Island (the closest to Jakarta) and 483cm2/months in the Belanda Island (the further site). The highest sponge growth rate occurred on T1-T2 during transitional season from rainy to dry. The lowest growth rate was observed on T3 during transitional season from dry to rainy. In general, prevalence percentage was higher in Belanda Island than in Dapur Island. This study showed a persistence invasion of encrusting T. hoshinota on coral reef ecosystem that may overcome the function and role of associated organisms.

Incursion of the killer sponge Terpios hoshinota Rützler & Muzik, 1993 on the coral reefs of the Lakshadweep archipelago, Arabian Sea

Our study documents the outbreak of a coral-killing sponge Terpios hoshinota in the coral reefs of Lakshadweep archipelago and highlights that it has further extended its territory into the isolated atolls of Arabian Sea and maybe a growing threat to the existing coral reefs in the region.

First Report of the Coral-Killing Sponge Terpios hoshinota Rützler and Muzik, 1993 in Western Australia: A New Threat to Kimberley Coral Reefs?

The cyanobacteriosponge Terpios hoshinota has been reported throughout the Indo-Pacific including the Great Barrier Reef, Australia. The species encrusts live coral, giant clams, and other benthos and can be a threat to benthic communities on coral reefs. The Kimberley region of Western Australia has some of the least impacted reefs globally. We report for the first time the presence of T. hoshinota in the eastern Indian Ocean on Kimberley inshore coral reefs. Given its invasive potential, reef health surveys should include this species, and monitoring approaches developed to audit the remote Kimberley for this and other invasive species.