Phylogenetic diversity of epibiotic bacteria in the accessory nidamental glands of squids (Cephalopoda: Loliginidae and Idiosepiidae)

Pichon, Delphine; Gaia, Valéria; Norman, Mark D.; Boucher-Rodoni, Renata

doi:10.1007/s00227-005-0014-5

Marine Biology

2005

DOI: 10.1007/s00227-005-0014-5

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Phylogenetic diversity of epibiotic bacteria in the accessory nidamental glands of squids (Cephalopoda: Loliginidae and Idiosepiidae)

Delphine Pichon

Valéria Gaia

Mark D. Norman

et al.

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Cited by 38 publications

(34 citation statements)

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“…previously isolated from biofilms developed at Port Shelter, Hong Kong (authors' unpubl. data), while the 3 clones for the biofilms developed under nutrient enrichment all showed high similarity (96%) to an unculturable epibiotic bacterium in squid accessory nidamental glands (Pichon et al 2005).Relative abundances of individual diatom taxa in biofilms developed under nutrient enrichment and control conditions were compared (Fig. 3).…”

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Nutrient effects on intertidal community: from bacteria to invertebrates

Chiu¹,

Zhang²,

Wang³

et al. 2008

Mar. Ecol. Prog. Ser.

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This study investigated the impacts of nutrient enrichment on intertidal biofilm microbial communities and on larval metamorphosis of invertebrates. We modulated the nutrient levels in the water column during biofilm development and examined the resulting biofilms for bacterial and diatom community composition using 2 DNA fingerprinting techniques and microscopic examination, respectively. Results of both terminal-restriction fragment length polymorphism (T-RFLP) and denaturing gradient gel electrophoresis (DGGE) analyses indicated that the nutrient enrichment treatment altered the biofilm bacterial communities relative to the control. Biofilms that had different microbial compositions were tested for their effects on larval metamorphosis of the polychaete Hydroides elegans, the barnacle Balanus amphitrite, and the slipper limpet Crepidula onyx. We showed that nutrient enrichment in the water column effectively changed the biofilm composition in ways that increased its inductiveness for larval metamorphosis of C. onyx and B. amphitrite, but not of H. elegans. This study highlights the apparent importance of nutrient enrichment in influencing the intertidal biofilm composition directly and the invertebrates indirectly. KEY WORDS: Bacteria · Biofilms · Larvae · Nutrients Resale or republication not permitted without written consent of the publisherMar Ecol Prog Ser 358: [41][42][43][44][45][46][47][48][49][50] 2008 Although some attention has been paid to the direct inductive effects of nutrient enrichment on larval metamorphosis (e.g. Fitt & Coon 1992), there may be indirect effects of nutrient enrichment through biofilms. Whether nutrient enrichment is effective in changing the biofilm composition in ways that alter its effects on larval metamorphosis remains unknown. Furthermore, it was demonstrated that nutrient enrichment could cause changes in the composition of intertidal communities even though the mechanisms underlying those changes were not understood (e.g. Morris & Keough 2003). Therefore, our objective was to investigate the role of nutrients on biofilms, and consequently on the metamorphosis of invertebrate larvae, which affects the recruitment process and hence the composition of intertidal communities.In this study, we developed biofilms in the field under nutrient enrichment and control conditions; the nutrient levels in the water column were modulated by using a fertilizer which releases a cocktail of nutrients that are representative of those being transferred to coastal areas (Morris & Keough 2003). Because of the importance of bacteria and diatoms on larval metamorphosis (e.g. Qian et al. 2003, Lau et al. 2005, Chiu et al. 2007), resulting biofilms were examined for diatom and bacterial cell densities and community composition. Then we tested the effects of the biofilms on larval metamorphosis of the polychaete Hydroides elegans, the barnacle Balanus amphitrite, and the slipper limpet Crepidula onyx. Biofilms are one of the key natural inductive cues for the larval metamorphosis of...

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confidence: 99%

Nutrient effects on intertidal community: from bacteria to invertebrates

Chiu¹,

Zhang²,

Wang³

et al. 2008

Mar. Ecol. Prog. Ser.

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“…Sexually mature females of some species have an accessory nidamental gland (ANG), a reproductive organ that houses a dense consortium of bacteria in pigmented epithelium-lined tubules and is attached to the nidamental gland (NG), the organ that secretes the jelly coat surrounding fertilized eggs (6). Culture-dependent and -independent methods have identified the dominant members of these microbial communities for some squid species (3,6,25,39). All squid ANGs examined to date are dominated by alphaproteobacteria, usually members of the Roseobacter clade within the Rhodobacterales (6,16,39) with additional members belonging to the Gammaproteobacteria (vibrios, pseudoalteromonads, and pseudomonads) and the Bacteroidetes.…”

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confidence: 99%

“…Culture-dependent and -independent methods have identified the dominant members of these microbial communities for some squid species (3,6,25,39). All squid ANGs examined to date are dominated by alphaproteobacteria, usually members of the Roseobacter clade within the Rhodobacterales (6,16,39) with additional members belonging to the Gammaproteobacteria (vibrios, pseudoalteromonads, and pseudomonads) and the Bacteroidetes. Similar taxonomic groups were also found in the egg casings of the squid Loligo pealei, suggesting that the ANG serves to inoculate the egg clutches with a bacterial population (6).…”

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confidence: 99%

Diversity and Partitioning of Bacterial Populations within the Accessory Nidamental Gland of the Squid Euprymna scolopes

Collins

LaBarre

Won

et al. 2012

Appl Environ Microbiol

117

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ABSTRACTMicrobial consortia confer important benefits to animal and plant hosts, and model associations are necessary to examine these types of host/microbe interactions. The accessory nidamental gland (ANG) is a female reproductive organ found among cephalopod mollusks that contains a consortium of bacteria, the exact function of which is unknown. To begin to understand the role of this organ, the bacterial consortium was characterized in the Hawaiian bobtail squid,Euprymna scolopes, a well-studied model organism for symbiosis research. Transmission electron microscopy (TEM) analysis of the ANG revealed dense bacterial assemblages of rod- and coccus-shaped cells segregated by morphology into separate, epithelium-lined tubules. The host epithelium was morphologically heterogeneous, containing ciliated and nonciliated cells with various brush border thicknesses. Hemocytes of the host's innate immune system were also found in close proximity to the bacteria within the tubules. A census of 16S rRNA genes suggested thatRhodobacterales, Rhizobiales, andVerrucomicrobiabacteria were prevalent, with members of the genusPhaeobacterdominating the consortium. Analysis of 454-shotgun sequencing data confirmed the presence of members of these taxa and revealed members of a fourth,Flavobacteriaof theBacteroidetesphylum. 16S rRNA fluorescentin situhybridization (FISH) revealed that many ANG tubules were dominated by members of specific taxa, namely,Rhodobacterales,Verrucomicrobia, orCytophaga-Flavobacteria-Bacteroidetes, suggesting symbiont partitioning to specific host tubules. In addition, FISH revealed that bacteria, includingPhaeobacterspecies from the ANG, are likely deposited into the jelly coat of freshly laid eggs. This report establishes the ANG of the invertebrateE. scolopesas a model to examine interactions between a bacterial consortium and its host.

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“…Stappia stellulata and Stappia aggregata were originally isolated from coastal marine water column and sediment samples, assigned to the genus Agrobacterium, and subsequently transferred to the genus Stappia (1,29,38). Stappia alba (27), Stappia marina (9), and various Stappia-like isolates have since been obtained from numerous widely distributed sources, including warm temperate surface and permanently cold deep-sea waters, sediments, phytoplankton, macroalgae, invertebrates, and salt marshes (2,3,5,9,13,17,26,27,33; Donachie et al, unpublished data). In addition, the presence of Stappia or Stappia-like taxa in a similar range of habitats has also been inferred from cultivation-independent analyses (3,26;Donachie et al,unpublished).…”

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Physiological, Ecological, and Phylogenetic Characterization of Stappia , a Marine CO-Oxidizing Bacterial Genus

Weber

King

2007

Appl Environ Microbiol

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Bacteria play a major role in marine CO cycling, yet very little is known about the microbes involved. Thirteen CO-oxidizing Stappia isolates obtained from existing cultures, macroalgae, or surf samples representing geographically and ecologically diverse habitats were characterized using biochemical, physiological, and phylogenetic approaches. All isolates were aerobic chemoorganotrophs that oxidized CO at elevated (1,000 ppm) and ambient-to-subambient concentrations (<0.3 ppm). All contained the form I (OMP) coxL gene for aerobic CO dehydrogenase and also the form II (BMS) putative coxL gene. In addition, some strains possessed cbbL, the large subunit gene for ribulose-1,5-bisphosphate carboxylase/oxygenase, suggesting the possibility of lithotrophic or mixotrophic metabolism. All isolates used a wide range of sugars, organic acids, amino acids, and aromatics for growth and grew at salinities from 5 to 45 ppt. All but one isolate denitrified or respired nitrate. Phylogenetic analyses based on 16S rRNA gene sequences indicated that several isolates could not be distinguished from Stappia aggregata and contributed to a widely distributed species complex. Four isolates (of strains GA15, HI, MIO, and M4) were phylogenetically distinct from validly described Stappia species and closely related genera (e.g., Ahrensia, Pannonibacter, Pseudovibrio, and Roseibium). Substrate utilization profiles, enzymatic activity, and membrane lipid composition further distinguished these isolates and supported their designations as new Stappia species. The observed metabolic versatility of Stappia likely accounts for its cosmopolitan distribution and its ability to contribute to CO cycling as well as other important biogeochemical cycles.

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Phylogenetic diversity of epibiotic bacteria in the accessory nidamental glands of squids (Cephalopoda: Loliginidae and Idiosepiidae)

Cited by 38 publications

References 23 publications

Nutrient effects on intertidal community: from bacteria to invertebrates

Nutrient effects on intertidal community: from bacteria to invertebrates

Diversity and Partitioning of Bacterial Populations within the Accessory Nidamental Gland of the Squid Euprymna scolopes

Physiological, Ecological, and Phylogenetic Characterization of Stappia , a Marine CO-Oxidizing Bacterial Genus

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