Development of the Accessory Nidamental Gland and Associated Bacterial Community in the Hawaiian Bobtail Squid, <i>Euprymna scolopes</i>

Kerwin, Allison H.; McAnulty, Sarah J.; Nyholm, Spencer V.

doi:10.1086/713965

Cited by 14 publications

(31 citation statements)

References 43 publications

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“…It has been previously shown through fluorescence in situ hybridization that different bacterial taxa in the ANG are observed in separate tubules ( Collins et al, 2012 ). It has also been seen that the relative abundance of different bacterial classes shift as the ANG develops, which occurs as the nascent gland tissue forms pores that lead to invaginations that will become tubules in the mature gland ( Kerwin et al, 2021 ). Similar to the light organ crypts, where T6SS2-dependent competition shapes the diversity and spatial arrangement of V. fischeri strains, the ANG tubules would provide a similar niche for ANG symbiont competition during colonization.…”

Section: Discussionmentioning

confidence: 99%

Prevalence and diversity of type VI secretion systems in a model beneficial symbiosis

et al. 2022

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The type VI secretion system (T6SS) is widely distributed in diverse bacterial species and habitats where it is required for interbacterial competition and interactions with eukaryotic cells. Previous work described the role of a T6SS in the beneficial symbiont, Vibrio fischeri, during colonization of the light organ of Euprymna scolopes squid. However, the prevalence and diversity of T6SSs found within the distinct symbiotic structures of this model host have not yet been determined. Here, we analyzed 73 genomes of isolates from squid light organs and accessory nidamental glands (ANGs) and 178 reference genomes. We found that the majority of these bacterial symbionts encode diverse T6SSs from four distinct classes, and most share homology with T6SSs from more distantly related species, including pathogens of animals and humans. These findings indicate that T6SSs with shared evolutionary histories can be integrated into the cellular systems of host-associated bacteria with different effects on host health. Furthermore, we found that one T6SS in V. fischeri is located within a genomic island with high genomic plasticity. Five distinct genomic island genotypes were identified, suggesting this region encodes diverse functional potential that natural selection can act on. Finally, analysis of newly described T6SSs in roseobacter clade ANG isolates revealed a novel predicted protein that appears to be a fusion of the TssB-TssC sheath components. This work underscores the importance of studying T6SSs in diverse organisms and natural habitats to better understand how T6SSs promote the propagation of bacterial populations and impact host health.

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Section: Discussionmentioning

confidence: 99%

Prevalence and diversity of type VI secretion systems in a model beneficial symbiosis

et al. 2022

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“…This bacterial consortium within the ANG is populated via horizontal transmission from the marine environment (Kaufman et al, 1998;Li et al, 2019). Although the bacterial consortia of ANGs show variety in different species (Collins et al, 2012;Kerwin and Nyholm, 2017;Yang et al, 2021), its composition shifts gradually during female maturation (Kerwin et al, 2021;Yang et al, 2021). The dynamics of the bacterial consortium in the ANG appear to comprise an intricate process governed by host selection during female maturation.…”

Section: Introductionmentioning

confidence: 99%

“…A single symbiotic bacterial species (V. fischeri) produces bioluminescence in the light organ of the Hawaiian bobtail squid which is controlled by a daily biological rhythm through the quorum-sensing system (Boettcher et al, 1996;Lupp et al, 2003). On the contrary, a complex consortium of microbes synthesizes carotenoids (pigments) which accumulate in the ANG at the time of female maturation (Lum- Kong and Hastings, 1992;Kerwin et al, 2021;Yang et al, 2021). As a result, the color of the ANG changes from white to yellow, orange, and red during sexual maturation in female squids (Bloodgood, 1977;Li et al, 2019;Li et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

“…The bigfin reef squid belongs to Myopsida, which possess only the ANG organ; the light organ is absent in this species (Lindgren et al, 2012). The development of the ANGs has been previously studied in female bigfin reef squid (Li et al, 2019) and other coleoid cephalopods (Lum- Kong, 1992;Kaufman et al, 1998;Kerwin et al, 2021). During ANG development, the bacteria are gradually transferred from the outer epithelial cells layers by environmental microbiota; these cell layers are deeply invaginated and form tubule structures in the inner epithelial cell layers for bacterial flora (Lum- Kong, 1992;Kaufman et al, 1998;Li et al, 2019;Kerwin et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

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Transcriptomic profile of symbiotic accessory nidamental gland during female maturation in bigfin reef squid

Tseng

Li²,

Chen³

et al. 2023

Front. Mar. Sci.

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The bigfin reef squid, Sepioteuthis lessoniana, are a valuable commercial species in East Asian regions such as Taiwan and Japan. A lack of genomic information limits the application of potential aquaculture techniques, especially in breeding when considering the hatching rate of offspring. In some squids and cuttlefishes, symbiotic bacteria are transmitted from the accessory nidamental gland (ANG) to the jelly coat of eggs. In Hawaiian bobtail squid, these parent-delivered mutualistic bacteria play an important role in preventing lethal biofouling of the eggs and accelerating the hatch rate of offspring. The bacterial consortium, which is housed in the female squids ANG, are governed by host selection during female maturation. Immune functions are typically used to explain the regulatory mechanism of symbioses by host selection. In this study, we evaluated the transcripts featured in bacterial selection and maintenance during ANG development using RNA-seq. Different developmental stages of ANGs (stages 1–4) were sequenced. The de novo transcriptome assembly resulted in 524,918 unigenes. Two groups, non-pigmentation group (stage 1 and stage 3) and pigmentation group (stage 4), were clustered by transcriptome-wide expression profile analysis. The gene expression analyses indicated that 9,475 differential expression genes (DEGs) in three different phases and 1,363 (14.3%) DEGs were matched in the Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) databases. Furthermore, KEGG-enriched analysis results suggested that immune responses are a dominant pathway in the non-pigmentation group (stage 1 and stage 3) whereas lipid metabolism and metabolism of flora fermentation are dominant in the pigmentation group (stage 4). Although the host immunity plays an important role during bacterial colonization of the ANG in bigfin reef squid, our results showed that most immune-related genes had a reduced transcriptomic level in the pigmentation group compared with the non-pigmentation group. Therefore, our results provide new insight to understand the regulatory mechanisms of initial bacterial colonization and later bacterial pigmentation in the bigfin reef squid.

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“…Several species such as the Hawaiian bobtail squid (Euprymna scolopes) have been cultured as model organisms for studying developmental biology, neurobiology, gene regulation, cospeciation, and various aspects of behavior and physiology (Hanlon et al, 1997;Kerwin et al, 2021;Montague et al, 2021;Zepeda et al, 2017).…”

Section: Cephalopoda As a Model Taxon For Invertebrate Bioacousticsmentioning

confidence: 99%

Assessing anthropogenic noise impacts and relevant soundscape cues for marine invertebrates: leveraging squid and coral reefs as model systems

Jones¹

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Sound is utilized by marine animal taxa for many ecologically important functions, and these taxa are vulnerable to adverse effects of anthropogenic noise on hearing and behavior. However, little is known about marine invertebrates’ responses to anthropogenic noise, and the ambient environmental sounds (“soundscapes”) they detect and respond to. Most acoustic studies report sound pressure (detected by mammals and some fish), but few report particle motion, the back-and-forth vibratory component of sound detected by marine invertebrates. I investigated invertebrate use of and response to sounds in two facets: 1) behavioral responses of longfin squid, Doryteuthis pealeii to anthropogenic noise, and 2) particle motion of coral reef soundscapes in the U.S. Virgin Islands. In laboratory-based experiments I exposed D. pealeii to construction noise originally recorded from an offshore wind farm. I found significant increases in squids’ alarm responses and in failed prey capture attempts during noise. Conversely, noise exposure had no significant effects on reproductive behaviors of groups of D. pealeii, indicating high motivation of these squid to reproduce during this stressor. Collectively, these experiments revealed the importance of considering behavioral context in studies and regulatory decisions regarding invertebrates’ susceptibility to anthropogenic noise impacts. In studying coral reef soundscapes, I reported particle motion trends over several months for coral reefs varying in habitat quality, including coral cover and fish abundance. I found acoustic properties over which particle motion closely scaled with pressure, and others over which it did not. I compared soundscape data with particle motion hearing thresholds, and found that invertebrates may only detect high amplitude and low frequency transient sound cues on reefs, such as those produced by fishes. My research bring new insights on natural and anthropogenic sound cues detectable by marine invertebrates, and how and when invertebrates will be vulnerable to anthropogenic noise pollution.

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Development of the Accessory Nidamental Gland and Associated Bacterial Community in the Hawaiian Bobtail Squid, Euprymna scolopes

Cited by 14 publications

References 43 publications

Prevalence and diversity of type VI secretion systems in a model beneficial symbiosis

Prevalence and diversity of type VI secretion systems in a model beneficial symbiosis

Transcriptomic profile of symbiotic accessory nidamental gland during female maturation in bigfin reef squid

Assessing anthropogenic noise impacts and relevant soundscape cues for marine invertebrates: leveraging squid and coral reefs as model systems

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