The Evolution, Assembly, and Dynamics of Marine Holobionts

Annual Review of Marine Science, Journal Year: 2023, Volume and Issue: 16(1), P. 443 - 466

Published: Aug. 8, 2023

The holobiont concept (i.e., multiple living beings in close symbiosis with one another and functioning as a unit) is revolutionizing our understanding of biology, especially marine systems. earliest was likely syntrophic partnership at least two prokaryotic members. Since then, has enabled organisms to conquer all ocean habitats through the formation holobionts wide spectrum complexities. However, most scientific inquiries have focused on isolated their adaptations specific environments. In this review, we attempt illustrate why perspective-specifically, study how numerous form discrete ecological unit symbiosis-will be more impactful strategy advance ecology evolution life. We argue that approach instrumental addressing threats biodiversity posed by current global environmental crisis.

Language: Английский

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Extracellular symbiont colonizes insect during embryo development

ISME Communications, Journal Year: 2024, Volume and Issue: 4(1)

Published: Jan. 1, 2024

Abstract Insects typically acquire their beneficial microbes early in development. Endosymbionts housed intracellularly are commonly integrated during oogenesis or embryogenesis, whereas extracellular only known to be acquired after hatching by immature instars such as larvae nymphs. Here, however, we report on an symbiont that colonizes its host embryo Tortoise beetles (Chrysomelidae: Cassidinae) digestive bacterial Stammera extracellularly within foregut symbiotic organs and ovary-associated glands ensure vertical transmission. We outline the initial stages of colonization observe although develop 3 days prior larval emergence, they remain empty until final 24 h Infection occurs timeframe hatching. By experimentally manipulating availability embryos egg, describe a 12-h developmental window governing Stammera. Symbiotic form normally aposymbiotic larvae, demonstrating these Stammera-bearing structures autonomously. In adults, already colonized following metamorphosis stable population facilitate folivory. The glands, initially lack Symbiont abundance subsequently increases transmission organs, thereby ensuring sufficient titers at onset oviposition ~29 metamorphosis. Collectively, our findings reveal precedes where proliferation is eventually decoupled adult match nutritional reproductive requirements host.

Language: Английский

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Impact of modeled microgravity stress on innate immunity in a beneficial animal-microbe symbiosis

Scientific Reports, Journal Year: 2024, Volume and Issue: 14(1)

Published: Feb. 5, 2024

Abstract The innate immune response is the first line of defense for all animals to not only detect invading microbes and toxins but also sense interface with environment. One such environment that can significantly affect immunity spaceflight. In this study, we explored impact microgravity stress on key elements NFκB pathway. symbiosis between bobtail squid Euprymna scolopes its beneficial symbiont Vibrio fischeri was used as a model system under simulated expression genes associated pathway monitored over time progressed. Results revealed although onset major driver in differential signaling, low-shear caused dysregulation expression. Several were expressed at earlier points suggesting E. are stress-inducible, whereas other components delayed. results provide new insights into role signaling squid-vibrio symbiosis, how negatively impacts host response. Together, these foundation develop mitigation strategies maintain host-microbe homeostasis during

Language: Английский

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Evolutionary history influences the microbiomes of a female symbiotic reproductive organ in cephalopods

Applied and Environmental Microbiology, Journal Year: 2024, Volume and Issue: unknown

Published: Feb. 5, 2024

ABSTRACT Many female squids and cuttlefishes have a symbiotic reproductive organ called the accessory nidamental gland (ANG) that hosts bacterial consortium involved with egg defense against pathogens fouling organisms. While ANG is found in multiple cephalopod families, little known about global microbial diversity of these symbionts. We used 16S rRNA gene community analysis to characterize microbiome from different species assess relationship between host symbiont phylogenies. The 11 cephalopods four families (superorder: Decapodiformes) span seven geographic locations was characterized. Bacteria class Alphaproteobacteria, Gammaproteobacteria , Flavobacteriia were all species, yet amplicon sequence variants by distance metrics revealed significant difference microbiomes (weighted/unweighted UniFrac, Bray–Curtis, P = 0.001). Despite being collected widely disparate locations, members family Sepiolidae (bobtail squid) shared many taxa including (~50%) Opitutae (Verrucomicrobia) Ruegeria (Alphaproteobacteria) species. Furthermore, we tested for phylosymbiosis positive correlation phylogenetic dissimilarity (Mantel test r 0.7). These data suggest closely related sepiolids select distinct symbionts similar taxa. Overall, ANGs harbor thus offer diverse explore antimicrobial activity other functional roles fitness. IMPORTANCE aquatic organisms recruit environment provide variety functions, pathogens. Some (squids, bobtail squids, cuttlefish) contains protects eggs wide distribution cephalopods, whether they share unknown. Here, studied distributed over broad range representing 15–120 million years divergence. some taxa, but each had unique members. Additionally, host–symbiont phylogenies suggests evolutionary histories partners been important shaping microbiome. This study advances our knowledge cephalopod–bacteria relationships provides foundation defensive systems.

Language: Английский

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Euprymna berryias a comparative model host forVibrio fischerilight organ symbiosis

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2025, Volume and Issue: unknown

Published: Jan. 13, 2025

ABSTRACT Functional studies of host-microbe interactions benefit from natural model systems that enable exploration molecular mechanisms at the interface. Bioluminescent Vibrio fischeri colonize light organ Hawaiian bobtail squid, Euprymna scolopes , and this binary has enabled advances in understanding communication, colonization specificity, vivo biofilms, intraspecific competition, quorum sensing. The hummingbird berryi, can be generationally bred maintained lab settings had multiple genes deleted by CRISPR approaches. prospect expanding utility system producing multigenerational host lines led us to determine extent which E. berryi symbiosis parallels known processes . However, nature organ, including its microbial constituency specificity for partners, have not been examined. In report, we isolate bacteria animals tank water. Assays bacterial behaviors required host, as well responses colonization, illustrate largely parallel phenotypes hatchlings. This study reveals a valuable comparative complement IMPORTANCE Microbiome substantially advanced functional interrogation roles partners communication between those partners. scolopes-Vibrio contributed foundational knowledge, revealing key sensing broadly animal hosts, stimulating development, motility accessing sites, biofilm formation development an animal’s microbiome. is second squid one recently shown robust laboratory husbandry amenable gene knockout. identifies strong due features are conserved with will extension symbioses.

Language: Английский

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Cassiopea xamachana microbiome across anatomy, development, and geography

PLoS ONE, Journal Year: 2025, Volume and Issue: 20(4), P. e0319944 - e0319944

Published: April 11, 2025

The upside-down jellyfish holobiont, Cassiopea xamachana , is a useful model system for tri-partite interactions between the cnidarian host, photosymbiont, and bacterial microbiome. While interaction host photosymbiont has been well studied, less understood of associated community. To date, microbiome wild C. remained largely uncharacterized. Thus, medusae (n=6) larvae (n=3) were collected from two sites in Florida Keys. Bacterial community composition was characterized via amplicon sequencing 16S rRNA gene V4 region. medusa dominated by members Alphaproteobacteria Gammaproteobacteria, while Planctomycetota, Actinomycetota, Bacteroidota, Bacillota also present, among others. Community consistent locations across structures (oral arm, bell, gonad). larval clustered apart beta diversity analysis presence several Pseudomonadota taxa that not present medusa, including Alteromonas Pseudoalteromonas Thalassobius genera. A isolate library encompassing much developed tested metabolic assays separate culture-dependent isolates bells, oral arms, laplets. Most characteristics correlated with sex or structure, but gelatinase production more common laplet isolates, lactose fermentation female arm isolates. Endozoicomonas genus dominant both our library, equally prevalent all sexes. Understanding component holobiont will allow us to further develop this important holobiont.

Language: Английский

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Microbial diversity and pigment synthesis in the accessory nidamental gland: species-specific and color-associated patterns in bigfin reef squid (Sepioteuthis lessoniana)

Animal Microbiome, Journal Year: 2025, Volume and Issue: 7(1)

Published: April 12, 2025

In certain cephalopod species, two distinct symbiotic organs host large populations of microorganisms: the light organ, regulated by daily cycle, and accessory nidamental gland (ANG), female reproductive cycle. While host-microbiota interactions in organ bobtail squid are well understood, dynamics within ANG remain largely unexplored. This study uses bigfin reef squid, Sepioteuthis lessoniana, as a model to investigate microbiomes associated with specific regions ANG, capitalizing on its relatively size compared squid. Our goal was characterize species-specific explore how pigmented region-dependent microbes contribute fitness Histological results indicate that four types epithelial cells were observed secondary tubules inner layer. Using an amplicon-based approach, we found Alphaproteobacteria highly abundant different species. Beta diversity analyses revealed significant interspecies differences microbiomes, while alpha showed harbored richer bacterial community than other Notably, exhibited lower microbial whole tissues, significantly enriched these regions. Hyphomicrobiaceae (Alphaproteobacteria) unique orange regions, Fodinicurvataceae Flavobacteriaceae (Bacteroidia) exclusive white qPCR higher transcription levels immune response-associated genes region suggesting localized interactions. These findings suggest Alphaproteobacteria, particularly clade, may correlated synthesis pigmentation The roles symbiosis still needs further investigation. With this knowledge, propose investigations using situ hybridization detect host-expressed bacteria markers. approach will facilitate providing deeper insights into mechanism host-microbe communication.

Language: Английский

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Organ structure and bacterial microbiogeography in a reproductive organ of the Hawaiian bobtail squid reveal dimensions of a defensive symbiosis

Applied and Environmental Microbiology, Journal Year: 2025, Volume and Issue: unknown

Published: April 15, 2025

ABSTRACT Many plants and animals house symbiotic microorganisms in specialized tissues or organs. Here, we used multidimensional situ imaging techniques to illuminate how host organ structure bacterial microbiogeography contribute the function of an Hawaiian bobtail squid, Euprymna scolopes . Along with well-studied light organ, female E. harbor a community bacteria accessory nidamental gland (ANG). The ANG is dense network epithelium-lined tubules, some which are dominated by single taxon. These deposited into squid eggs, where they defend developing embryos from harmful biofouling. This study combination visualize different dimensions its communities. Imaging entire organs sheet microscopy revealed that composite tissue individual, non-intersecting tubules each their own population. bisected, converging toward two points at posterior end. At these points, empty space can mix jelly be onto eggs. Observations correlated taxa cell morphology tubule populations varied: contained mixed taxa, whereas others only one genus. Together, data shed on interact within uses physical maintain employ population defensive context. IMPORTANCE Sequence-based microbiome studies have much about hosts communities microbiota but often lack spatial understanding microbes relate other reside. reveal , houses diverse, beneficial deploys them for egg defense. findings suggest partitioning may key harboring diverse antimicrobial-producing establishing foundation further structures mediate interactions.

Language: Английский

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The buzz within: the role of the gut microbiome in honeybee social behavior

Journal of Experimental Biology, Journal Year: 2024, Volume and Issue: 227(3)

Published: Feb. 1, 2024

ABSTRACT Gut symbionts influence the physiology and behavior of their host, but extent to which these effects scale social behaviors is an emerging area research. The use western honeybee (Apis mellifera) as a model enables researchers investigate gut microbiome at several levels organization. Insight into microbial societal level critical for our understanding how involved are in host biology. In this Commentary, we discuss recent findings research synthesize with knowledge other organisms hypothesize host–microbe interactions individual could shape dynamics evolution.

Language: Английский

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Host–symbiont plasticity in the upside-down jellyfish Cassiopea xamachana: strobilation across symbiont genera

Frontiers in Ecology and Evolution, Journal Year: 2024, Volume and Issue: 12

Published: March 14, 2024

Introduction In the upside-down jellyfish, Cassiopea xamachana (Cnidaria: Scyphozoa), establishment of photosymbiosis with dinoflagellates (family Symbiodiniaceae) is necessary for sessile polyp to undergo metamorphosis (strobilation) into a free-swimming adult. C. has capacity associate wide variety dinoflagellate species and representatives divergent genera. While some studies have looked at successful induction symbiosis, none date examined lasting effect diverse symbiont taxa on host survivorship development, which needed assess fitness costs such symbioses. Methods Our study exposes polyps 22 different cultured Symbiodinaceae strains representing 13 from 5 We analyzed time strobilation, number ephyra (juvenile medusa) produced, proportion that died prematurely. Results Here we show strobilation can be induced by nearly each symbiodinacean strain tested, exception free-living (i.e., unknown establish symbiosis any other marine host). Additionally, ephyrae did not display morphological variation or differences varying symbionts. However, observed intraspecific in induce strains. Discussion This work expands known form stable mutualisms , primarily genera Symbiodinium Breviolum . provide evidence ability symbiodiniaceans host, suggests population-level cultures impact their success. By utilizing an animal like flexible uptake, are able explore how diversity influence timing success symbiosis-driven development.

Language: Английский

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