Sex- and age-specific mercury accumulation in a long-lived seabird.

Mercury levels in the environment are increasing, such that they are also expected to accumulate in top-predators, but individual-based longitudinal studies required to investigate this are rare. Between 2017 and 2023, we therefore collected 1314 blood samples from 588 individual common terns (Sterna hirundo) to examine how total blood mercury concentration changed with age, and whether this differed between the sexes. Blood mercury concentrations were highly variable, but all exceeded toxicity thresholds above which adverse health effects were previously observed. A global model showed blood mercury to be higher in older birds of both sexes. Subsequent models partitioning the age effect into within- and among-individual components revealed a linear within-individual accumulation with age in females, and a decelerating within-individual accumulation with age in males. Time spent at the (particularly contaminated) breeding grounds prior to sampling, as well as egg laying in females, were also found to affect mercury concentrations. As such, our study provides evidence that male and female common terns differentially accumulate mercury in their blood as they grow older and calls for further studies of the underlying mechanisms as well as its consequences for fitness components, such as reproductive performance and survival.

Benthic microbial biogeographic trends in the North Sea are shaped by an interplay of environmental drivers and bottom trawling effort.

Microbial composition and diversity in marine sediments are shaped by environmental, biological, and anthropogenic processes operating at different scales. However, our understanding of benthic microbial biogeography remains limited. Here, we used 16S rDNA amplicon sequencing to characterize benthic microbiota in the North Sea from the top centimeter of 339 sediment samples. We utilized spatially explicit statistical models, to disentangle the effects of the different predictors, including bottom trawling intensity, a prevalent industrial fishing practice which heavily impacts benthic ecosystems. Fitted models demonstrate how the geographic interplay of different environmental and anthropogenic drivers shapes the diversity, structure and potential metabolism of benthic microbial communities. Sediment properties were the primary determinants, with diversity increasing with sediment permeability but also with mud content, highlighting different underlying processes. Additionally, diversity and structure varied with total organic matter content, temperature, bottom shear stress and bottom trawling. Changes in diversity associated with bottom trawling intensity were accompanied by shifts in predicted energy metabolism. Specifically, with increasing trawling intensity, we observed a transition toward more aerobic heterotrophic and less denitrifying predicted metabolism. Our findings provide first insights into benthic microbial biogeographic patterns on a large spatial scale and illustrate how anthropogenic activity such as bottom trawling may influence the distribution and abundances of microbes and potential metabolism at macroecological scales.

Abundance, biomass and species richness of macrozoobenthos along an intertidal elevation gradient.

Ecology aims to comprehend species distribution and its interaction with environmental factors, from global to local scales. While global environmental changes affect marine biodiversity, understanding the drivers at smaller scales remains crucial. Tidal flats can be found on most of the world's coastlines and are particularly vulnerable to anthropogenic disturbances. They are important transient ecosystems between terrestrial and marine ecosystems, and their biodiversity provides important ecosystem services. Owing to this unique, terrestrial-marine transition, strong environmental gradients of elevation, sediment composition and food availability prevail. Here, we investigated which regional and local environmental factors drive the spatio-temporal dynamics of macrozoobenthos communities on back-barrier tidal flats in the East Frisian Wadden Sea. On the regional level, we found that species composition changed significantly from west to east on the East Frisian islands and that total abundance and species richness decreased from west to east. On the local abiotic level, we found that macrozoobenthos biomass decreased with higher elevation towards the salt marsh and that the total abundance of organisms in the sediment significantly increased with increasing mud content, while biodiversity and biomass were not changing significantly. In contrast to expectations, increasing Chl a availability as a measure of primary productivity did not result in changes in abundance, biomass or biodiversity, but extremely high total organic carbon (TOC) content was associated with a decrease in biomass and biodiversity. In conclusion, we found regional and local relationships that are similar to those observed in previous studies on macrozoobenthos in the Wadden Sea. Macrozoobenthos biomass, abundance and biodiversity are interrelated in a complex way with the physical, abiotic and biotic processes in and above the sediment.

Mass mortality event of the giant barrel sponge Xestospongia sp.: population dynamics and size distribution in Koh Phangan, Gulf of Thailand.

Marine sponges are prominent organisms of the benthic coral reef fauna, providing important ecosystem services. While there have been increasing reports that sponges are becoming one of the dominant benthic organisms in some locations and ecoregions (e.g. Caribbean), they can be impacted by changing environmental conditions. This study presents the first documentation of a mass mortality event of the barrel sponge Xestospongia sp. in the lower Gulf of Thailand and its consequences on population dynamics and size distribution. Two anthropogenic impacted reefs (Haad Khom and Mae Haad) of the island Koh Phangan and two anthropogenic non-impacted reefs of the islands Koh Yippon and Hin Yippon within the Mu Ko Ang Thong Marine National Park were surveyed in the years 2015 and 2016. The results showed a strong shift in population densities at Koh Phangan. Fatal "bleaching" ending up in mass mortality was observed for these reefs in 2015. Xestospongia sp. abundance decreased from 2015 to 2016 by 80.6% at Haad Khom and by 98.4% at Mae Haad. Sponges of all sizes were affected, and mortality occurred regardless of the survey depth (4 and 6 m). However, Xestospongia population densities in the Marine Park were at a constant level during the surveys. The abundances in 2015 were 65% higher at the Marine Park than at Koh Phangan and 92% higher in 2016. The most likely causes of the mass mortality event was a local harmful algal bloom event, pathogens, undetected local higher water temperatures, or a combination of these factors, whereas sea surface temperature analyses showed no marine heatwave during the observed mass mortality event in 2015. Considering the ecological importance of sponges such as Xestospongia sp., long-term monitoring of reefs and their environmental parameters should be implemented to prevent such mass die-offs.

Ecotoxicological Effects of Four Commonly Used Organic Solvents on the Scleractinian Coral Montipora digitata.

Organic solvents are often used in aquatic toxicity tests to facilitate the testing of hydrophobic or poorly water-soluble substances such as ultraviolet (UV) filters, pesticides, or polycyclic aromatic hydrocarbons (PAHs). Knowledge of intrinsic effects (i.e., measured as standardized and non-standardized endpoints) of such carrier solvents in non-standardized organisms (i.e., corals), is critical to regulatory processes. Therefore, we exposed the reef-building coral Montipora digitata to the most commonly used carrier solvents ethanol, methanol, dimethyl sulfoxide, and dimethylformamide in the range of 10-100 µL L-1 for 16 days. The effects on mortality, photobiological, morphological, and oxidative stress markers were evaluated. In our study, all solvents resulted in significant morphological and/or oxidative stress responses, but not in mortality. Moreover, ethanol led to a rapid increase in turbidity, thus questioning its suitability as a carrier solvent in aquatic studies in general. Based on our observations, we could rank the solvent effects as follows: dimethylformamide < dimethyl sulfoxide ≈ methanol ≤ ethanol, with dimethylformamide showing the least and ethanol the most pronounced effects. We conclude that the use of solvents in toxicity studies with corals, particularly by examining non-standardized (e.g., morphological, physiological) endpoints, should be taken with caution and requires further elaboration.

Photodegradation of a bacterial pigment and resulting hydrogen peroxide release enable coral settlement.

The global degradation of coral reefs is steadily increasing with ongoing climate change. Yet coral larvae settlement, a key mechanism of coral population rejuvenation and recovery, is largely understudied. Here, we show how the lipophilic, settlement-inducing bacterial pigment cycloprodigiosin (CYPRO) is actively harvested and subsequently enriched along the ectoderm of larvae of the scleractinian coral Leptastrea purpura. A light-dependent reaction transforms the CYPRO molecules through photolytic decomposition and provides a constant supply of hydrogen peroxide (H2O2), leading to attachment on the substrate and metamorphosis into a coral recruit. Micromolar concentrations of H2O2 in seawater also resulted in rapid metamorphosis, but without prior larval attachment. We propose that the morphogen CYPRO is responsible for initiating attachment while simultaneously acting as a molecular generator for the comprehensive metamorphosis of pelagic larvae. Ultimately, our approach opens a novel mechanistic dimension to the study of chemical signaling in coral settlement and provides unprecedented insights into the role of infochemicals in cross-kingdom interactions.

Acute Toxicity Assays with Adult Coral Fragments: A Method for Standardization.

Coral reefs are globally declining due to various anthropogenic stressors. Amongst those, chemical pollutants, such as pesticides from agricultural runoff, sewage or an overabundance of personal care products in coastal waters due to intense tourism, may be considered as a local stressor for reef-building corals. The extent to which such chemicals exhibit toxic effects towards corals at environmentally relevant concentrations is currently controversially discussed and existing studies are often based on varying and sometimes deficient test methods. To address this uncertainty, we adapted available methods into a reliable and comprehensive acute coral toxicity test method for the reef-building coral Montipora digitata. The toxicities of the four substances benzophenone-3 (BP-3), Diuron (DCMU), copper (Cu2+ as CuCl2, positive control) and dimethylformamide (DMF, solvent) were assessed in a 96 h semi-static test design. Endpoints such as maximum quantum yield, bleaching, tissue loss and mortality were evaluated with respect to their suitability for regulatory purposes. Overall, the endpoints bleaching and mortality yielded sensitive and robust results for the four tested substances. As the test method follows the principles of internationally standardized testing methods (ISO, OECD), it can be considered suitable for further validation and standardization. Once validated, a standardized test method will help to obtain reproducible toxicity results useful for marine hazard and risk assessment and regulatory decision making.

Biodiversity, environmental drivers, and sustainability of the global deep-sea sponge microbiome.

In the deep ocean symbioses between microbes and invertebrates are emerging as key drivers of ecosystem health and services. We present a large-scale analysis of microbial diversity in deep-sea sponges (Porifera) from scales of sponge individuals to ocean basins, covering 52 locations, 1077 host individuals translating into 169 sponge species (including understudied glass sponges), and 469 reference samples, collected anew during 21 ship-based expeditions. We demonstrate the impacts of the sponge microbial abundance status, geographic distance, sponge phylogeny, and the physical-biogeochemical environment as drivers of microbiome composition, in descending order of relevance. Our study further discloses that fundamental concepts of sponge microbiology apply robustly to sponges from the deep-sea across distances of >10,000 km. Deep-sea sponge microbiomes are less complex, yet more heterogeneous, than their shallow-water counterparts. Our analysis underscores the uniqueness of each deep-sea sponge ground based on which we provide critical knowledge for conservation of these vulnerable ecosystems.

Mercury contamination level is repeatable and predicted by wintering area in a long-distance migratory seabird.

The environmental presence of mercury has dramatically increased over the past century, leading to increased uptake, especially by top predators such as seabirds. Understanding the exact sources of contamination requires an individual-level approach, which is especially challenging for species that migrate. We took such an approach and located the wintering areas of 80 common terns (Sterna hirundo) through tracking, and, across years, collected feathers grown in those areas to assess their mercury levels using atomic absorption spectrometry. Although feathers of males and females did not differ in their mercury level, we found the average feather mercury level to be highest in birds wintering in the Canary Current (3.87 µg g-1), medium in birds wintering in the Guinea Current (2.27 µg g-1) and lowest in birds wintering in the Benguela Current (1.96 µg g-1). Furthermore, we found considerable inter-annual fluctuations in feather mercury levels, a within-individual repeatability of 41%, that the mercury levels of 17% of feather samples exceeded the admitted toxicity threshold of 5 µg g-1, and that the overall mean concentration of 3.4 µg g-1 exceeded that of other published reports for the species. Further studies therefore should assess whether these levels lead to individual-level carry-over effects on survival and reproductive performance.

Winogradskyella luteola sp.nov., Erythrobacter ani sp. nov., and Erythrobacter crassostrea sp.nov., isolated from the hemolymph of the Pacific Oyster Crassostrea gigas.

Three new bacterial strains, WHY3T, WH131T, and WH158T, were isolated and described from the hemolymph of the Pacific oyster Crassostrea gigas utilizing polyphasic taxonomic techniques. The 16S rRNA gene sequence analysis revealed that strain WHY3T was a member of the genus Winogradskyella, whereas strains WHI31T and WH158T were members of the genus Erythrobacter. According to the polygenomic study the three strains formed individual lineages with strong bootstrap support. The comparison of dDDH-and ANI values, percentage of conserved proteins (POCP), and average amino acid identity (AAl) between the three strains and their relatives established that the three strains represented two separate genera. Menaquinone-6 was reported as the major respiratory quinone in strain WHY3T and Ubiquinone-10 for strains WH131T and WH158T, respectively. The major cellular fatty acids for strain WHY3T were C15:0, anteiso-C15:1 ω7c, iso-C15:0, C16:1ω7c. The major cellular fatty acids for strains WH131T and WH158T were C14:02-OH and t18:1ω12 for WH131T and C17:0, and C18:1ω7c for strain WH158T. Positive Sudan Black B staining Indicated the presence of polyhydroxyalkanoic acid granules for strains WH131T and WH158T but not for strain WHY3T. The DNA G + C contents of strains WHY3T, WH131T and WH158T were 34.4, 59.7 and 56.6%, respectively. Gene clusters predicted some important genes involved in the bioremediation process. Due to the accomplishment of polyphasic taxonomy, we propose three novel species Winogradskyella luteola sp.nov. (type strain WHY3T = DSM 111804T = NCCB 100833T), Erythrobacter ani sp.nov. (WH131T = DSM 112099T = NCCB 100824T) and Erythrobacter crassostrea sp.nov. (WH158T = DSM 112102T = NCCB 100877T).

Exploring the Antibiotic Production Potential of Heterotrophic Bacterial Communities Isolated from the Marine Sponges Crateromorpha meyeri, Pseudaxinella reticulata, Farrea similaris, and Caulophacus arcticus through Synergistic Metabolomic and Genomic Analyses.

The discovery of novel secondary metabolites is actively being pursued in new ecosystems. Sponge-associated bacteria have been in the limelight in recent years on account of their ability to produce bioactive compounds. In this study, heterotrophic bacteria associated with four sponge species were isolated, taxonomically identified, and subjected to screening for the production of bioactive entities against a panel of nine microorganisms, including Gram-positive and negative bacteria, as well as yeast and fungi. Of the 105 isolated strains, 66% were represented by Proteobacteria, 16% by Bacteriodetes, 7% by Actinobacteria, and 11% by Firmicutes. Bioactivity screening revealed that 40% of the total isolated strains showed antimicrobial activity against one or more of the target microorganisms tested. Further, active extracts from selective species were narrowed down by bioassay-guided fractionation and subsequently identified by HR-ESI-MS analyses to locate the active peaks. Presumably responsible compounds for the observed bioactivities were identified as pentadecenoic acid, oleic acid, and palmitoleic acid. One isolate, Qipengyuania pacifica NZ-96T, based on 16S rRNA novelty, was subjected to comparative metabolic reconstruction analysis with its closest phylogenetic neighbors, revealing 79 unique functional roles in the novel isolate. In addition, genome mining of Qipengyuania pacifica NZ-96T revealed three biosynthetic gene clusters responsible for the biosynthesis of terpene, beta lactone, lasso peptide, and hserlactone secondary metabolites. Our results demonstrate the ability to target the sponge microbiome as a potential source of novel microbial life with biotechnological potential.

Photobacterium arenosum WH24, Isolated from the Gill of Pacific Oyster Crassostrea gigas from the North Sea of Germany: Co-cultivation and Prediction of Virulence.

Cream colored bacteria from marine agar, strain WH24, WH77, and WH80 were isolated from the gill of the Crassostrea gigas a Pacific oyster with a filter-feeding habit that compels accompanying bacteria to demonstrate a high metabolic capacity, has proven able to colonize locations with changing circumstances. Based on the 16S rRNA gene sequence, all strains had high similarity to Photobacterium arenosum CAU 1568T (99.72%). This study involved phenotypic traits, phylogenetic analysis, antimicrobial activity evaluation, genome mining, Co-cultivation experiments, and chemical studies of crude extracts using HPLC and LC-HRESIMS. Photobacterium arenosum WH24 and Zooshikella harenae WH53Twere co-cultivated for 3 days in a rotary shaker at 160 rpm at 30 °C, and LC-MS monitored the chemical profiles of the co-cultures on the third day. The UV chromatograms of the extracts of the co-cultivation experiments show that Zooshikella harenae WH53T could be inhibited by strain WH24. The high virulence of Photobacterium arenosum WH24 was confirmed by genome analysis. Gene groups with high virulence potential were detected: tssA (ImpA), tssB (ImpB/vipA), tssC (ImpC/vipB), tssE, tssF (ImpG/vasA), tssG (ImpH/vasB), tssM (IcmF/vasK), tssJ (vasD), tssK (ImpJ/vasE), tssL (ImpK/vasF), clpV (tssH), vasH, hcp, lapP, plpD, and tpsB family.

Population genetics and demography of the coral-killing cyanobacteriosponge, Terpios hoshinota, in the Indo-West Pacific.

The first occurrence of the cyanobacteriosponge Terpios hoshinota was reported from coral reefs in Guam in 1973, but was only formally described in 1993. Since then, the invasive behavior of this encrusting, coral-killing sponge has been observed in many coral reefs in the West Pacific. From 2015, its occurrence has expanded westward to the Indian Ocean. Although many studies have investigated the morphology, ecology, and symbiotic cyanobacteria of this sponge, little is known of its population genetics and demography. In this study, a mitochondrial cytochrome oxidase I (COI) fragment and nuclear ribosomal internal transcribed spacer 2 (ITS2) were sequenced to reveal the genetic variation of T. hoshinota collected from 11 marine ecoregions throughout the Indo-West Pacific. Both of the statistical parsimony networks based on the COI and nuclear ITS2 were dominated by a common haplotype. Pairwise F ST and Isolation-by-distance by Mantel test of ITS2 showed moderate gene flow existed among most populations in the marine ecoregions of West Pacific, Coral Triangle, and Eastern Indian Ocean, but with a restricted gene flow between these regions and Maldives in the Central Indian Ocean. Demographic analyses of most T. hoshinota populations were consistent with the mutation-drift equilibrium, except for the Sulawesi Sea and Maldives, which showed bottlenecks following recent expansion. Our results suggest that while long-range dispersal might explain the capability of T. hoshinota to spread in the IWP, stable population demography might account for the long-term persistence of T. hoshinota outbreaks on local reefs.

Light Availability Affects the Symbiosis of Sponge Specific Cyanobacteria and the Common Blue Aquarium Sponge (Lendenfeldia chondrodes).

Bacterial symbionts in marine sponges play a decisive role in the biological and ecological functioning of their hosts. Although this topic has been the focus of numerous studies, data from experiments under controlled conditions are rare. To analyze the ongoing metabolic processes, we investigated the symbiosis of the sponge specific cyanobacterium Synechococcus spongiarum and its sponge host Lendenfeldia chondrodes under varying light conditions in a defined aquarium setting for 68 days. Sponge clonal pieces were kept at four different light intensities, ranging from no light to higher intensities that were assumed to trigger light stress. Growth as a measure of host performance and photosynthetic yield as a proxy of symbiont photosynthetic activity were measured throughout the experiment. The lack of light prevented sponge growth and induced the expulsion of all cyanobacteria and related pigments by the end of the experiment. Higher light conditions allowed rapid sponge growth and high cyanobacteria densities. In addition, photosynthetically active radiation above a certain level triggered an increase in cyanobacteria's lutein levels, a UV absorbing protein, thus protecting itself and the host's cells from UV radiation damage. Thus, L. chondrodes seems to benefit strongly from hosting the cyanbacterium S. spongiarum and the relationship should be considered obligatory mutualistic.

Towards the Development of Standardized Bioassays for Corals: Acute Toxicity of the UV Filter Benzophenone-3 to Scleractinian Coral Larvae.

Coral reefs have been declining globally at a historically unprecedented rate. Ultraviolet (UV) filters used in sunscreens may contribute to this decline at local scales, which has already led to bans on various organic UV filters in some regions. However, the underlying studies for these bans demonstrated significant flaws in the experimental design due to a lack of validated and standardized testing methods for corals. This study aimed to investigate options for the development of a standard acute toxicity test for the larval stage of scleractinian corals. Planula larvae of two brooding (Leptastrea purpurea and Tubastraea faulkneri) and two spawning (Acropora digitifera and A. millepora) species were exposed to the organic UV filter benzophenone-3 (BP3) for 48 h under static conditions. We observed interspecific variations in toxicity, with A. digitifera being the most sensitive (LC50 = 0.75 µg L-1) and T. faulkneri the least sensitive (LC50 = 2951.24 µg L-1) species. Inhibition of settlement was found to be a useful endpoint leading to an EC50 of 1.84 µg L-1 in L. purpurea larvae. Although the analytical challenges of measuring lipophilic substances in small volume test setups remain, the here applied test design and selected endpoints are suitable for further validation and subsequent standardization.

A comprehensive approach to assess marine macro litter pollution and its impacts on corals in the Bangka Strait, North Sulawesi, Indonesia.

This is a comprehensive study showing the marine anthropogenic litter pollution within North Sulawesi, Indonesia. From an area of 2972 m2 that encompassed five sparsely populated locations, a total of 9421 litter items weighing 137 kg were collected. One location (Talisei North) contributed 50% of all collected litter items. Plastic litter always dominated with 96-99%. Litter was unevenly distributed across investigated areas reaching from the upper beach (3.6-30.1 items/m2) to the reef slope (0-0.03 items/m2). Litter composition and daily accumulation showed spatial-temporal dynamics, with upper beach areas displaying the overall highest accumulation rates. Reef micro-habitats were differently affected, with the reef moat and reef flat showing the highest litter concentrations, although litter amounts were much lower compared to the corresponding beaches. Branching corals, especially Porites cylindrica, were most affected by litter entanglement. Field experiments with P. cylindrica showed that attached plastic induced bleaching, necrosis, and algal overgrowth within five months.

Characterization of an Insoluble and Soluble Form of Melanin Produced by Streptomyces cavourensis SV 21, a Sea Cucumber Associated Bacterium.

Melanin is a widely distributed and striking dark-colored pigment produced by countless living organisms. Although a wide range of bioactivities have been recognized, there are still major constraints in using melanin for biotechnological applications such as its fragmentary known chemical structure and its insolubility in inorganic and organic solvents. In this study, a bacterial culture of Streptomyces cavourensis SV 21 produced two distinct forms of melanin: (1) a particulate, insoluble form as well as (2) a rarely observed water-soluble form. The here presented novel, acid-free purification protocol of purified particulate melanin (PPM) and purified dissolved melanin (PDM) represents the basis for an in-depth comparison of their physicochemical and biological properties, which were compared to the traditional acid-based precipitation of melanin (AM) and to a synthetic melanin standard (SM). Our data show that the differences in solubility between PDM and PPM in aqueous solutions may be a result of different adjoining cation species, since the soluble PDM polymer is largely composed of Mg2+ ions and the insoluble PPM is dominated by Ca2+ ions. Furthermore, AM shared most properties with SM, which is likely attributed to a similar, acid-based production protocol. The here presented gentler approach of purifying melanin facilitates a new perspective of an intact form of soluble and insoluble melanin that is less chemical altered and thus closer to its original biological form.

Coral reef benthic community changes in the Anthropocene: Biogeographic heterogeneity, overlooked configurations, and methodology.

Non-random community changes are becoming more frequent in many ecosystems. In coral reefs, changes towards communities dominated by other than hard corals are increasing in frequency, with severe impacts on ecosystem functioning and provision of ecosystem services. Although new research suggests that a variety of alternative communities (i.e. not dominated by hard corals) exist, knowledge on the global diversity and functioning of alternative coral reef benthic communities, especially those not dominated by algae, remains scattered. In this systematic review and meta-analysis of 523 articles, we analyse the different coral reef benthic community changes reported to date and discuss the advantages and limitations of the methods used to study these changes. Furthermore, we used field cover data (1116 reefs from the ReefCheck database) to explore the biogeographic and latitudinal patterns in dominant benthic organisms. We found a mismatch between literature focus on coral-algal changes (over half of the studies analysed) and observed global natural patterns. We identified strong biogeographic patterns, with the largest and most biodiverse biogeographic regions (Western and Central Indo-Pacific) presenting previously overlooked soft-coral-dominated communities as the most abundant alternative community. Finally, we discuss the potential biases associated with methods that overlook ecologically important cryptobenthic communities and the potential of new technological advances in improving monitoring efforts. As coral reef communities inevitably and swiftly change under changing ocean conditions, there is an urgent need to better understand the distribution, dynamics as well as the ecological and societal impacts of these new communities.

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

Terpios hoshinota is an aggressive, space-competing sponge that kills various stony corals. Outbreaks of this species have led to intense damage to coral reefs in many locations. Here, the first large-scale 16S rRNA gene survey across three oceans revealed that bacteria related to the taxa Prochloron, Endozoicomonas, SAR116, Ruegeria, and unclassified Proteobacteria were prevalent in T. hoshinota. A Prochloron-related bacterium was the most dominant and prevalent cyanobacterium in T. hoshinota. The complete genome of this uncultivated cyanobacterium and pigment analysis demonstrated that it has phycobiliproteins and lacks chlorophyll b, which is inconsistent with the definition of Prochloron. Furthermore, the cyanobacterium was phylogenetically distinct from Prochloron, strongly suggesting that it should be a sister taxon to Prochloron. Therefore, we proposed this symbiotic cyanobacterium as a novel species under the new genus Candidatus Paraprochloron terpiosi. Comparative genomic analyses revealed that 'Paraprochloron' and Prochloron exhibit distinct genomic features and DNA replication machinery. We also characterized the metabolic potentials of 'Paraprochloron terpiosi' in carbon and nitrogen cycling and propose a model for interactions between it and T. hoshinota. This study builds a foundation for the study of the T. hoshinota microbiome and paves the way for better understanding of ecosystems involving this coral-killing sponge.