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Schupp, P. J.

Publications and source records attributed to Schupp, P. J..

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Benthic macrofauna and microbiota mediate bottom trawling impacts on long-term carbon storage in marine sediments

The seafloor is the largest organic carbon sink on Earth. Its benthic fauna and microbiota jointly regulate long-term carbon storage by assimilating and degrading sedimentary organic matter (SOM). Bottom trawling threatens the long-term storage of organic matter by physical disturbance of the seafloor and remobilization of SOM. Trawling also impacts faunal and microbial communities and their diversity, but the implications of these ecological consequences for long-term carbon storage dynamics are poorly understood. Here, we combined datasets of paired faunal and microbial communities from the North Sea and used structural equation modeling to disentangle direct and biotically mediated effects of bottom trawling on SOM. One third of trawling-induced SOM loss is indirect and mediated by shifts in benthic faunal and microbial communities. Microbial community structure directly affected SOM and represented a key link in this pathway. Microbial effects on SOM were strongly tied to changes in metabolic traits. SOM loss coincides with increased microbial aerobic respiration potential, whereas SOM increases correlated with microbial assimilation processes, including dark carbon fixation. Benthic fauna impact SOM indirectly by shaping benthic microbial communities. Faunal diversity and species traits related to bioturbation promoted shifts in benthic microbiota that favor OM storage, corroborating their indirect but essential role in seafloor carbon dynamics. This study reveals that bottom trawling alters seafloor carbon storage not only through physical disturbance but also by disrupting faunal-microbial interactions that regulate sediment carbon dynamics. Taxonomic and functional shifts in benthic microbiota are a key, but underestimated, component of the processes regulating the seafloor carbon sink and warrant better integration of benthic biodiversity and ecological processes into assessments of seafloor carbon storage under anthropogenic pressures.

ecology↗

Flatfish intestinal microbiota depend on various host traits, and vary with sediment type and bottom trawling effort

The intestinal microbiota of fishes support digestion, nutrient uptake and play an important role in the immune system, development and reproduction. Flatfish live in close contact with the seafloor, and are particularly exposed to anthropogenic disturbances such as bottom trawling. Bottom trawling impacts the ecosystem in various ways and it recent evidence indicates that the microbial composition and diversity in marine sediments varies with fishing intensity. It is presently unknown whether this trawling signal applies to the seafloor alone, or may also extend to microbiota of marine holobionts inhabiting it, such as flatfishes. Here, three flatfish species (Buglossidium luteum, Limanda limanda and Pleuronectes platessa) were sampled across the southeastern North Sea. We characterized the intestinal microbiota using 16S rDNA metabarcoding of 162 individuals, and disentangled how intestinal microbial composition and diversity are jointly shaped by various host traits (species, sex, age, weight, and condition factor) and environmental factors (sediment type and trawling intensity). Intestinal diversity varied among species and changed with age, weight and sediment type. Community composition was dependent on species, age, condition factor and sediment type. In addition, we found that trawling intensity explained shifts in intestinal microbial community composition, suggesting that the known impacts of bottom trawling on the benthic environment may cascade to intestinal microbiota of flatfish. Our findings provide important insight into host-microbiota interactions in marine ecosystems and highlight the interplay between host traits and environment as drivers of intestinal microbial diversity and community composition in flatfish. HighlightsO_LIFlatfish microbiota are shaped by host traits and environmental factors C_LIO_LIHost species and age affect intestinal microbial diversity and composition C_LIO_LIIntestinal microbiota vary along a bottom trawling intensity gradient C_LIO_LIBottom trawling impacts may cascade from sediments to fish intestinal microbiota C_LI

ecology↗

Dissolved organic matter fluxes and fatty acid composition from shallow-water and deep-water demo- and hexactinellid sponges from New Zealand

Sponges are an important component of shallow- and deep-water ecosystems enhancing eukaryotic biodiversity via diverse endo- and epibiota and by providing three dimensional habitats for benthic invertebrates and fishes. Sponge biodiversity is particularly high in the waters around New Zealand (Southwest Pacific), where we collected two shallow- and two deep-water sponge species (Tedania sp., Suberea meandrina, Farrea raoulensis, Artemisina sp.) for ex-situ incubation experiments to detect whether these sponges may process dissolved organic matter. We assessed the biochemical and phospholipid-derived fatty acids (PLFAs) and measured dissolved organic carbon (DOC) and total dissolved nitrogen (TDN) fluxes. Changes in fluorescent dissolved organic matter (FDOM) over time were analyzed and the results were linked to the bacterial communities of the sponge holobiont. Dried sponge tissue consisted of 17.5 {+/-} 3.75% organic (org.) C and of 4.34 {+/-} 1.02% total nitrogen (TN) with a natural stable isotope composition of -19.0 {+/-}0.25{per thousand} for {delta}13org. C and of 10.2 {+/-}2.43{per thousand} for {delta}15TN. None of the DOC fluxes was significant and only the release of TDN by Tedania sp. was significantly different from 0 mol TDN g org. C-1 d-1. We detected the presence of four fluorophores in the FDOM pool: 2 tryptophan- and protein-like fluorophores (C1, C2), 1 humic-like fluorophore (C3), and 1 tyrosine-like fluorophore (C4). The maximum fluorescence intensity Fmax of C1 decreased significantly in S. meandrina incubations, whereas Fmax of C2 grew in the same incubations. Fmax of C3 increased in Tedania sp. incubations, in which Fmax of C4 decreased. In comparison, Fmax of C4 in S. meandrina rose. The PLFA composition of sponge tissue was dominated by long-chain fatty acids, saturated fatty acids, and monosaturated fatty acids and most PLFAs were sponge- and bacteria-specific. The bacterial community of the demosponges Artemisina sp., S. meandrina and Tedania sp. consisted mostly of Proteobacteria and Chloroflexota, whereas the dominating bacteria phylum of the hexactinellid F. raoulensis was Proteobacteria. We proposed that the holobionts of S. meandrina and Tedania sp. contain bacteria that are involved in the transformation and degradation of DOM. In S. meandrina, Chloroflexota and Poribacteria may degrade tryptophan-like fluorophores to a chemically modified tryptophan-like and protein-like fluorophore, while producing a tyrosine-like fluorophore. In Tedania sp., Chloroflexota may contribute to the release of significant amounts of TDN by producing humic-like fluorophores, while degrading tyrosine-like fluorophores. Farrea raoulensis may not take up DOM due to a lack of Poribacteria and Chloroflexota or may use colloidal instead of truly dissolved DOC.

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Nutrient fluxes, oxygen consumption and fatty acid composition from deep-water demo- and hexactinellid sponges from New Zealand

Sponges are an important component of deep-water ecosystems enhancing eukaryotic biodiversity by hosting diverse endo- and epibiota and providing three dimensional habitats for benthic invertebrates and fishes. As holobionts they are important hosts of microorganisms which are involved in carbon and nitrogen cycling. While increasing exploration of deep-water habitats results in new sponge species being discovered, little is known about their physiology and role in nutrient fluxes. Around New Zealand (Southwest Pacific), the sponge biodiversity is particularly high, and we selected six deep-sea sponge clusters (Saccocalyx, Suberites, Tedania, Halichondria/ Dendoricella, Sceptrulophora, Lissodendoryx) for in-situ and ex-situ experiments. We investigated the biochemical composition of the sponges, measured oxygen consumption and inorganic nutrient fluxes, as well as bacterial and phospholipid-derived fatty acid (PLFA) compositions. Our aim was to assess differences in fluxes and fatty acid composition among sponge clusters and linking their bacterial communities to nitrogen cycling processes. All sponges excreted nitrite and ammonia. Nitrate and phosphate excretion were independent of phylum affiliation (Demospongiae, Hexactinellida). Nitrate was excreted by the Halichondria/ Dendoricella and Lissodendoryx clusters, whereas the Suberites, Tedania, and Sceptrulophora clusters consumed it. Phosphate was excreted by Sceptrulophora and Halichondria/ Dendoricella clusters and consumed by all other clusters. Silicon was consumed by all sponge clusters, except for Saccocalyx and Halichondria/ Dendoricella clusters. Oxygen consumption rates ranged from 0.17 to 3.56{+/-}0.60 mmol O2 g C d-1. The PLFA composition was very sponge-cluster dependent and consisted mostly of long-chain fatty acids. Most PLFAs were sponge-specific, followed by bacteria-specific PLFAs, and others. All sponge clusters, except for Suberites, were low-microbial abundance (LMA) sponges whose bacterial community composition was dominated by Proteobacteria, Bacteroidota, Planctomycetota, and Nitrospinota. The Suberites cluster consisted of high-microbial abundance (HMA) sponges with Proteobacteria, Chloroflexota, Acidobacteriota, and Actinobacteriota as dominant bacteria. Based on the inorganic nitrogen flux measurements, we identified three types of nitrogen cycling in the sponges: In type 1, sponges (Dendoricella spp. indet., Lissodendoryx cluster) respired aerobically and ammonificated organic matter (OM) to ammonium, fixed N2 to ammonium, and nitrified aerobically heterotrophically produced ammonium to nitrate and nitrite. In type 2, sponges (Halichondria sp., Sceptrulophora, Suberites, Tedania clusters) respired OM aerobically and ammonificated it to ammonium. They also reduced nitrate anaerobically to ammonium via dissimilatory nitrate reduction to ammonium. In type 3, ammonium was microbially nitrified to nitrite and afterwards to nitrate presumably by ammonium-oxidizing Bacteria and/ or Archaea.

ecology↗

From microbial communities to regional biogeography: Unraveling patterns, determinants and the influence of bottom trawling in benthic microbiota

Microbial composition and diversity in marine sediments are shaped by environmental, biological, and anthropogenic processes that operate on different scales. However, our understanding of benthic microbial biogeography remains limited. Here, we study how benthic microbiota vary at a regional scale in the North Sea with sediment characteristics, temperature, organic matter content, shear bed stress and bottom trawling intensity, a prevalent industrial fishing practice which heavily impacts benthic ecosystems. Using 16S rDNA amplicon sequencing, we characterized benthic microbiota from the top centimeter of 349 sediment samples and used uni-and multivariate statistical models, accounting for spatial autocorrelation, to disentangle the effects of the different predictors. Fitted models demonstrate how the geographic interplay of different environmental anthropogenic drivers shapes the structure and functioning of benthic microbial communities. Sediment properties were the primary determinants, with diversity increasing with sediment permeability but at the same time increasing with mud content, highlighting different underlying processes. Alpha diversity also increased nonlinearly with total organic matter content and temperature and showed a more complex relationship with bottom shear stress but decreased with bottom trawling intensity. These trawling associated diversity changes were accompanied by shifts in functional groups related to energy metabolism. Specifically, with increasing trawling intensity, we observed a transition toward more aerobic heterotrophic and less denitrifying metabolism. Our findings provide first insights of 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 overall benthic metabolism at macroecological scales.

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Trade-offs in a reef-building coral after six years of thermal acclimation

Evidence is growing that reef-building corals have the capacity to acclimate to new and challenging thermal conditions by increasing their thermal resistance. This raises hopes for their future persistence in a warming world. However, potential trade-offs that accompany such resistance gains, have remained largely unexplored. We provide the first report on the physiological trade-offs in a globally abundant and ecologically relevant coral species (Pocillopora acuta), after a long-term exposure to an elevated temperature of 31 {degrees}C in comparison to conspecifics cultivated under a cooler control thermal regime. At both temperatures, corals consistently appeared to be visually healthy throughout a six-year period. At 31 {degrees}C, corals had increased metabolic rates (both respiration and photosynthesis) that resulted in higher biomass accumulation and total energy reserves compared to the corals from the ambient regime. Further, the composition of coral host tissues shifted in favor of lipid build-up, suggesting an altered mechanism of energy storage. The increase in biomass growth came at the cost of declining skeletal growth rates and the formation of higher density skeletons. In the long-term, this trade-off will result in lower extension rates that can entail major ramifications for future reef building processes and reef community composition. Moreover, symbionts at 31 {degrees}C were physiologically more compromised with overall lower energy reserves, possibly indicating a stronger exploitation by the host and potentially a lower stress resilience. Our study provides first insights into a successful thermal acclimation mechanism that involved the prioritization of energy storage over skeletal growth, entailing higher demands on the symbionts. Our observation in this 6-year study does not align with observations of short-term studies, where elevated temperatures caused a depletion of tissue lipids in corals, which highlights the importance of studying acclimation of organisms over their relevant biological scales. Further investigations into trade-offs at biologically relevant scales and how they unfold under an acute heat stress will help to provide a more comprehensive picture of the future coral reef trajectory. Importantly, these insights will also help improve interventions aimed at increasing the thermal resilience of corals which anticipate to use thermal preconditioning treatments for stress-hardening. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=96 SRC="FIGDIR/small/549699v2_ufig1.gif" ALT="Figure 1"> View larger version (29K): org.highwire.dtl.DTLVardef@139b33corg.highwire.dtl.DTLVardef@1264477org.highwire.dtl.DTLVardef@158f7c9org.highwire.dtl.DTLVardef@1f3c35a_HPS_FORMAT_FIGEXP M_FIG C_FIG

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The prevalence, predominance, and metabolic potentials of Candidatus Prochlorobium terpiosii 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. hoshinotas 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.

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Beyond coral-algal regimes: high taxonomic resolution surveys and trait-based analyses reveal multiple benthic regimes

As coral reef communities change and reorganise in response to anthropogenic and climate disturbances, there is a growing need of detecting and understanding the different emerging species regimes and their contribution to key ecosystem processes. Using a case study on coral reefs at the epicentre of tropical marine biodiversity (North Sulawesi), we explored how application of different biodiversity approaches (i.e. use of major taxonomic categories, high taxonomic resolution categories and trait-based approaches) affects the detection of distinct fish and benthic community assemblages. Our results show that using major categories (family level or above) to study coral reef communities fails to identify distinct regimes. We also show that for detection of different benthic regimes, especially communities dominated by non-coral organisms, monitoring of only scleractinian coral communities is insufficient, and that all types of benthic organisms (e.g. sponges, ascidians, soft corals, algae etc.) need to be considered. We have implemented for the first time, the use of a trait-based approach to study the functional diversity of whole coral reef benthic assemblages, which allowed us to detect five different community regimes, only one of which was dominated by scleractinian corals. We circumvented the challenge that for some benthic groups (e.g. sponges, ascidians or some soft corals) visual identification up to the species level is not possible, by identifying and categorising traits that can be applied to groups of similar organisms instead of specific species. Furthermore, by the parallel study of benthic and fish communities we provide new insights into key processes and functions that might dominate or be compromised in the different community regimes.

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