Prokaryotic, Fungal, and Unicellular Eukaryotic Core Communities Across Three Sympatric Marine Sponges From the Southwestern Atlantic Coast Are Dominated Largely by Deterministic Assemblage Processes DOI Creative Commons
Cristiane Cassiolato Pires Hardoim, Gisele Lôbo‐Hajdu, Márcio Reis Custódio

et al.

Frontiers in Microbiology, Journal Year: 2021, Volume and Issue: 12

Published: June 8, 2021

Marine sponges are known to harbor a diverse and complex microbiota; however, vast majority of surveys have been investigating the prokaryotic communities in north hemisphere Australia. In addition, mechanisms microbial community assembly poorly understood this pivotal player ecosystem. Thus, survey addressed holobiome sponge species São Paulo region (Brazil) for first time investigated contribution neutral niche processes prokaryotic, fungal, unicellular eukaryotic assemblage three sympatric Aplysina caissara, fulva, Tedania ignis along with environmental samples. The compositions associated detected samples were strikingly different. Remarkably, between 47 88% assigned operational taxonomic units (OTUs) specifically species. Moreover, around 77, 69, 53% unclassified OTUs from communities, respectively, showed less than 97% similarity well-known databases, suggesting that southwestern Atlantic coast an important source novelty. These values even higher, 80 61% OTUs, when excluding low abundance fungal datasets, respectively. Host major driver shaping sponge-associated community. Deterministic primarily responsible all species, while also A. caissara T. replicates, Most species-rich lineages found Northern seas many them might play essential roles symbioses, such as biosynthesis secondary metabolites exhibit antimicrobial antiviral activities, well provide protection against host predation. Overall, study microbiota was assembled by interactions deterministic-based manner; closely related shared strong phylogenetic signal their traits Brazilian reservoir novel

Language: Английский

Discovery of an Abundance of Biosynthetic Gene Clusters in Shark Bay Microbial Mats DOI Creative Commons

Ray Chen,

Hon Lun Wong, Gareth Kindler

et al.

Frontiers in Microbiology, Journal Year: 2020, Volume and Issue: 11

Published: Aug. 21, 2020

Microbial mats are geobiological multilayered ecosystems that have significant evolutionary value in understanding the evolution of early life on Earth. Shark Bay, Australia has some best examples modern microbial thriving under harsh conditions high temperatures, salinity, desiccation, and ultraviolet (UV) radiation. Microorganisms living extreme thought to potentially encode for secondary metabolites as a survival strategy. Many natural products encoded by grouping genes known biosynthetic gene clusters (BGCs). Natural diverse chemical structures functions which provide competitive advantages microorganisms can also biotechnology applications. In present study, diversity BGC were described detail first time from Bay mats. A total 1477 BGCs detected metagenomic data over 20 mm mat depth horizon, with surface layer possessing 200 containing highest relative abundance all layers. Terpene bacteriocin highly represented their proposed important roles ecosystem function these systems. Interestingly, novel Heimdallarchaeota Lokiarchaeota, two evolutionarily archaeal phyla not previously possess BGCs. This study provides new insights into how may enable communities adapt environments.

Language: Английский

Citations

65

Giant sponge grounds of Central Arctic seamounts are associated with extinct seep life DOI Creative Commons
Teresa Morganti, Beate M. Slaby, Anna de Kluijver

et al.

Nature Communications, Journal Year: 2022, Volume and Issue: 13(1)

Published: Feb. 8, 2022

Abstract The Central Arctic Ocean is one of the most oligotrophic oceans on Earth because its sea-ice cover and short productive season. Nonetheless, across peaks extinct volcanic seamounts Langseth Ridge (87°N, 61°E), we observe a surprisingly dense benthic biomass. Bacteriosponges are abundant fauna within this community, with mass 460 g C m −2 an estimated carbon demand around 110 yr −1 , despite export fluxes from regional primary productivity only sufficient to provide <1% required carbon. Observed sponge distribution, bulk compound-specific isotope data fatty acids suggest that microbiome taps into refractory dissolved particulate organic matter, including remnants seep community. metabolic profile bacteriosponge expressed genes indicate autotrophic symbionts contribute significantly assimilation. We hotspot ecosystem unique associated biota, once fueled by degassing mounts.

Language: Английский

Citations

36

High microbiome and metabolome diversification in coexisting sponges with different bio-ecological traits DOI Creative Commons
Valerio Mazzella, Antonio Dell’Anno, Néstor Etxebarría

et al.

Communications Biology, Journal Year: 2024, Volume and Issue: 7(1)

Published: April 8, 2024

Abstract Marine Porifera host diverse microbial communities, which influence metabolism and fitness. However, functional relationships between sponge microbiomes metabolic signatures are poorly understood. We integrate microbiome characterization, metabolomics predicted functions of four coexisting Mediterranean sponges – Petrosia ficiformis , Chondrosia reniformis Crambe crambe Chondrilla nucula . Microscopy observations reveal anatomical differences in densities. Microbiomes exhibit strong species-specific trends. C. shares many rare amplicon sequence variants (ASV) with the surrounding seawater. This suggests important inputs diversity acquired by selective horizontal acquisition. Phylum Cyanobacteria is mainly represented According to putative functions, P. functionally heterotrophic, while autotrophic. The species display distinct profiles at single compound level. molecular class level they share a “core metabolome”. Concurrently, we find global microbiome-metabolome association when considering all species. Within each still, sets microbe/metabolites identified driving multi-omics congruence. Our findings suggest that players may promote niche diversification, but also, analogous phenotypic patterns “symbiont evolutionary convergence” assemblages where holobionts co-exist same area.

Language: Английский

Citations

8

DNA ‐stable isotope probing (DNA‐SIP) identifies marine sponge‐associated bacteria actively utilizing dissolved organic matter (DOM) DOI Creative Commons
Sara Campana, Kathrin Busch, Ute Hentschel

et al.

Environmental Microbiology, Journal Year: 2021, Volume and Issue: 23(8), P. 4489 - 4504

Published: June 22, 2021

Sponges possess exceptionally diverse associated microbial communities and play a major role in (re)cycling of dissolved organic matter (DOM) marine ecosystems. Linking sponge-associated community structure with DOM utilization is essential to understand host-microbe interactions the uptake, processing, exchange resources. We coupled, for first time, DNA-stable isotope probing (DNA-SIP) 16S rRNA amplicon sequencing sponge holobiont identify which symbiotic bacterial taxa are metabolically active uptake. Parallel incubation experiments Plakortis angulospiculatus were amended equimolar quantities unlabelled (12 C) labelled (13 DOM. Seven sequence variants (ASVs), belonging phyla PAUC34f, Proteobacteria, Poribacteria, Nitrospirae, Chloroflexi, identified as consumers Our results support predictions that Chloroflexi capable degradation through heterotrophic carbon metabolism, while Nitrospirae may have potential mixotrophic metabolism. present new analytical application DNA-SIP detect substrate incorporation into complex provide experimental evidence links identity bacteria consumption

Language: Английский

Citations

35

How does heat stress affect sponge microbiomes? Structure and resilience of microbial communities of marine sponges from different habitats DOI Creative Commons
Paula De Castro-Fernández, Elisenda Ballesté, Carlos Angulo–Preckler

et al.

Frontiers in Marine Science, Journal Year: 2023, Volume and Issue: 9

Published: Jan. 19, 2023

Introduction Sponges are key components of marine benthic communities, providing many ecosystem functions and establishing close relationships with microorganisms, conforming the holobiont. These symbiotic microbiotas seem to be host species-specific highly diverse, playing roles in their sponge host. The effects elevated seawater temperature on sponges microbiota still poorly known, whether from polar areas more sensitive these impacts respect temperate tropical species is totally unknown. Methods We analyzed microbiomes different natural habitat after exposure heat stress aquaria by 16S rRNA amplicon sequencing (1) characterize covering a latitudinal gradient (polar, environments), (2) asses thermal microbial communities. Results Bacterial communities’ structure was also surrounding seawater. core microbiome maintained most stress, although they would recover normal conditions previous remains yet further investigated. observed increased abundances transient bacteria unknown origin exposed stress. Discussion Some may opportunistic that benefit stress-associated dysregulation occupying new niches According our results, Antarctic waters could resilient than sponges. Both composition changes produced quite species-specific, thus, depend species. Under global change scenario, will probably those suffering therefore dramatic for ecosystems since fundamental part them.

Language: Английский

Citations

16

Sponges and their prokaryotic communities sampled from a remote karst ecosystem DOI Creative Commons
Daniel F. R. Cleary, Yusheng Huang, Ana R. M. Polónia

et al.

Marine Biodiversity, Journal Year: 2024, Volume and Issue: 54(1)

Published: Jan. 18, 2024

Abstract Marine karst ecosystems exist at the land-sea interface and are characterised by underwater formations sculpted over time action of seawater. Submerged caves crevices these host a rich array marine life which sponges among most abundant diverse components. In present study, we describe elements sponge fauna sampled from unique ecosystem remote island, Orchid Island, off southeastern coast Taiwan. The study includes several understudied taxa, including sclerosponges ( Acanthochaetetes wellsi , Astrosclera willeyana ) lithistid species dark, shallow-water caves. Prokaryotic communities were obtained total 22 demosponge species, 11 potentially new to science. tetracladinid, lithistids harboured prokaryotic communities, clustered separately all other contrasting with non-tetracladinid, Vetulina incrustans . lithistids, furthermore, formed two distinct clusters Spirophorina suborder clustering apart those Astrophorina suborder. sclerosponge A. also community in terms composition five unique, OTUs relatively low sequence similarities organisms GenBank. All cave enriched SAR202 members, group bacteria known for their role degradation recalcitrant compounds. highest relative abundance was found We propose that Island may play an as-yet uncharted nutrient dynamics interface.

Language: Английский

Citations

5

Lifestyle of sponge symbiont phages by host prediction and correlative microscopy DOI Creative Commons
Martin T. Jahn, Tim Lachnit, Sebastian M. Markert

et al.

The ISME Journal, Journal Year: 2021, Volume and Issue: 15(7), P. 2001 - 2011

Published: Feb. 18, 2021

Bacteriophages (phages) are ubiquitous elements in nature, but their ecology and role animals remains little understood. Sponges represent the oldest known extant animal-microbe symbiosis associated with dense diverse microbial consortia. Here we investigate tripartite interaction between phages, bacterial symbionts, sponge host. We combined imaging bioinformatics to tackle important questions on who phage hosts what replication mode spatial distribution within animal is. This approach led discovery of distinct phage-microbe infection networks versus seawater microbiomes. A new correlative situ ('PhageFISH-CLEM') localised phages symbiont cells, also phagocytotically active cells. postulate that phagocytosis free virions by cells modulates phage-bacteria ratios ultimately controls dynamics. Prediction strategies indicated a pattern, where lysogeny dominates microbiome, likely fostered host-mediated virion clearance, while lysis seawater. Collectively, this work provides insights into sponges, highlighting importance animal-phage-bacterium interplay holobiont functioning. anticipate our will be instrumental further understanding viral cellular association hosts.

Language: Английский

Citations

30

Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts DOI Creative Commons
Shan Zhang, Weizhi Song, Louis‐Félix Nothias

et al.

Microbiome, Journal Year: 2022, Volume and Issue: 10(1)

Published: Feb. 1, 2022

Sponges are ancient sessile metazoans, which form with their associated microbial symbionts a complex functional unit called holobiont. rich source of chemical diversity; however, there is limited knowledge holobiont members produce certain metabolites and how they may contribute to interactions. To address this issue, we applied non-targeted liquid chromatography tandem mass spectrometry (LC-MS/MS) gas (GC-MS) either whole sponge tissue or fractionated cells from six different, co-occurring species.Several were commonly found enriched in tissue, supporting the notion that them. These include 2-methylbutyryl-carnitine, hexanoyl-carnitine various carbohydrates, be potential food sources for microorganisms, as well antagonistic compounds hymenialdisine eicosatrienoic acid methyl ester. Metabolites mostly observed antioxidant didodecyl 3,3'-thiodipropionate, docosatetraenoic acid, immune-suppressor phenylethylamide. This suggests these mainly produced by holobiont, potentially involved inter-microbial competitions defenses against intruding organisms.This study shows different functionality compartmentalized between hosts provides new insights into interactions underpin function holobionts. Video abstract.

Language: Английский

Citations

21

Single-cell metabolite detection and genomics reveals uncultivated talented producer DOI Creative Commons

Masato Kogawa,

Rimi Miyaoka,

Franziska Hemmerling

et al.

PNAS Nexus, Journal Year: 2022, Volume and Issue: 1(1)

Published: March 1, 2022

The production of bioactive metabolites is increasingly recognized as an important function host-associated bacteria. An example defensive symbiosis that might account for much the chemical richness marine invertebrates including sponges (Porifera), 1 oldest metazoans. However, most bacterial members sponge microbiomes have not been cultivated or sequenced, and therefore, remain unrecognized. Unequivocally linking metabolic functions to a cellular source in is, challenge. Here, we report analysis pipeline microfluidic encapsulation, Raman microscopy, integrated digital genomics (MERMAID) efficient identification uncultivated producers. We applied this method chemically rich bacteriosponge (sponge hosts community) Theonella swinhoei, previously shown contain 'Entotheonella' symbionts produce substances isolated from sponge. As exception, antifungal aurantosides had remained unassigned source. Raman-guided single-bacterial sequencing revealed cryptic, distinct multiproducer, 'Candidatus Poriflexus aureus' new Chloroflexi lineage aurantoside producer. Its exceptionally large genome contains numerous biosynthetic loci suggested even higher than appreciated. This study highlights importance complementary technologies uncover microbiome functions, reveals remarkable parallels between distantly related same host, adds functional support diverse prolific lineages being present microbial dark matter.

Language: Английский

Citations

21

Comparative genomics analyses of Actinobacteriota identify Golgi phosphoprotein 3 (GPP34) as a widespread ancient protein family associated with sponge symbiosis DOI Creative Commons
Cláudia N. Ferreira, Ilia Burgsdorf,

Tzipora Perez

et al.

Microbiome, Journal Year: 2025, Volume and Issue: 13(1)

Published: Jan. 7, 2025

Sponges harbor microbial communities that play crucial roles in host health and ecology. However, the genetic adaptations enable these symbiotic microorganisms to thrive within sponge environment are still being elucidated. To understand adaptations, we conducted a comparative genomics analysis on 350 genomes of Actinobacteriota, phylum commonly associated with sponges. Our uncovered several differences between free-living bacteria, including an increased abundance genes encoding prokaryotic defense systems (PDSs) eukaryotic-like proteins (ELPs) symbionts. Furthermore, identified GPP34 as novel symbiosis-related gene family, found two Actinobacteriota clades, but not their closely related relatives. Analyses broader set microbes showed members family also symbionts across 16 additional bacterial phyla. While were thought be restricted eukaryotes, our phylogenetic shows domain is all three domains life, suggesting its ancient origin. We show includes main structures: short form only long encompasses coupled cytochrome P450 domain, which exclusive bacteria. Given previous studies showing phosphatidylinositol-4-phosphate (PI4P)-binding protein eukaryotes other PI4P-binding from pathogens can interfere phagolysosome maturation, propose employ modulate phagocytosis colonize persist hosts.

Language: Английский

Citations

0