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Meiobenthic nematode Oncholaimus campylocercoides as a model in laboratory studies: selection, culture, and fluorescence microscopy after exposure to phenanthrene and chrysene

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Abstract

Numerous studies have focused on the response of meiofauna after exposure to polycyclic aromatic hydrocarbons (PAHs), but none has been devoted to their uptake into nematode body compartments. The present study monitored PAH uptake by Oncholaimus campylocercoides which was selected after 40 days in the laboratory through original protocols from natural sediments collected in the Old Harbor of Bizerte, Tunisia. To achieve the mono-species level, a grain size magnification was applied by gradually adding a biosubstrate made from either the crushed shells of Mytilus galloprovincialis or minced leaves of Posidonia oceanica. After selection, O. campylocercoides was cultured and fed with earthworm powder (560 mg.l-1). Thereafter, it was exposed for 3 weeks to phenanthrene and chrysene (38, 116, and 348 ppb). Fluorescence microscopy revealed higher intensities of PAHs at the spicules, mouths, and pharynges compared with the other organs considered. Moreover, the buccal fluorescence showed a significant correlation with that measured in the biosubstrate made with shells of M. galloprovincialis.

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References

  • Alkio M, Tabuchi TM, Wang X, Cólon-Carmona A (2005) Stress responses to polycyclic aromatic hydrocarbons in Arabidopsis include growth inhibition and hypersensitive response-like symptoms. J Exp Bot 56:2983–2994

    Article  CAS  Google Scholar 

  • Allouche M, Nasri A, Harrath AH, Mansour L, Beyrem H, Boufahja F (2020a) Experimental selection of Marylynnia puncticaudata (Cyatholaimidae, Nematoda) and effects of organic enrichment. Environ Sci Pollut Res DOI. https://doi.org/10.1007/s11356-020-11050-1

  • Allouche M, Hamdi I, Nasri A, Harrath AH, Mansour L, Beyrem H, Boufahja F (2020b) Laboratory bioassay exploring the effects of anti-aging skincare products on free-living marine nematodes: case study of collagen. Environ Sci Pollut Res 27:11403–11412

    Article  CAS  Google Scholar 

  • Armenteros M, Pérez-García JA, Ruiz-Abierno A, Díaz-Asencio L, Helguera Y, Vincx M, Decraemer W (2010) Effects of organic enrichment on nematode assemblages in a microcosm experiment. Marine Environmental Research 70(5):374–382

    Article  CAS  Google Scholar 

  • Barrett J (1982) Metabolic responses to anabiosis in the fourth-stage juveniles of Ditylenchus dipsaci (Nematoda). Proc R Soc Lond B 216:159–177

    Article  CAS  Google Scholar 

  • Bates PA, Dokurni P, Freemont PS, Sternberg MJE (1998) Conformational analysis of the first observed non-proline cis-peptide bond occurring within the complementarity determining region (CDR) of an antibody. J Mol Biol 284:549–555

    Article  CAS  Google Scholar 

  • Ben Saïd O, Louati H, Soltani A, Mahmoudi E, Cravo-Laureau C, Pringault O, Duran R, Aissa P (2012) Etude in vitro de l’impact de sédiments artificiellement contaminés par l’anthracène: effets sur les bactéries indigènes et les nématodes libres marins. Can J Civ Eng 39(5):556–564

    Article  Google Scholar 

  • Bettaieb F, Khiari R, Dufresne A, Mhenni MF, Putaux JL, Boufi S (2015) Nanofibrillar cellulose from Posidonia oceanica: Properties and morphological features. Industrial Crops and Products 72(15):97–106

    Article  CAS  Google Scholar 

  • Bezerra TN, Decraemer W, Eisendle-Flöckner U, Hodda M, Holovachov O (2019) Leduc D, iljutin D, Mokievsky V, Peña Santiago R, Sharma J, Smol N, Tchesunov A, Venekey V, Zeng Z, Vanreusel A. World Database of Nematodes, Nemys available at: http://nemys.ugent.be/

    Google Scholar 

  • Blaxter ML, De Ley P, Garey GR, Liu LX, Scheldeman P, Vierstraete A, Vanfleteren JR, Mackey LR, Dorris M, Frisse LM, Vida JT, Thomas WK (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392:71–75

  • Boufahja F, Hedfi A, Amorri J, Aïssa P, Beyrem H, Mahmoudi E (2011) Examination of the bioindicator potential of Oncholaimus campylocercoides (Nematoda, Oncholaimidae) from Bizerte bay (Tunisia). Ecol Indic 11:1139–1148

    Article  CAS  Google Scholar 

  • Boufahja F, Semprucci F (2015) Stress-induced selection of a single species from an entire meiobenthic nematode assemblage: is this possible using iron enrichment and does pre-exposure affect the ease of the process? Environ Sci Poll Res 22:1979–1998

    Article  CAS  Google Scholar 

  • Boufahja F, Semprucci F, Beyrem H (2016) An experimental protocol to select nematode species from an entire community using progressive sedimentary enrichment. Ecol Indic 60:292–309

    Article  Google Scholar 

  • Caldwell RL, Caprioli RM (2005) Tissue profiling by mass spectrometry: a review of methodology and applications. Mol Cell Proteomics. 4:394–401

    Article  CAS  Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Clarke KR, Gorley RN (2001) PRIMER v5: User manual/tutorial. PRIMER-E: Plymouth, UK 91p

  • Clarke KR, Warwick RM (2001) Change in Marine Communities: An Approach to Statistical Analysis and Interpretation, 2nd edn. PRIMER-E, Ltd., Plymouth Marine Laboratory, Plymouth

    Google Scholar 

  • Cobb NA (1931) The use of live nemas (Metoncholaimus pristiurus) in zoological courses in schools and colleges. Science 74:489–490

    Article  CAS  Google Scholar 

  • Cox GN (1992) Molecular and biochemical aspects of nematode collagens. J Parasitol 78:1–15

    Article  CAS  Google Scholar 

  • De Lange HJ, Sperber V, Peeters ET (2006) Avoidance of polycyclic aromatic hydrocarbon-contaminated sediments by the freshwater invertebrates Gammarus pulex and Asellus aquaticus. Environ Toxicol Chem 25:452–457

    Article  Google Scholar 

  • Dutta K, Ghosh D, Nazmi A, Kumawat KL, Basu A (2010) A common carcinogen benzo[a]pyrene causes neuronal death in mouse via microglial activation. PloS ONE 5(4):e9984

    Article  Google Scholar 

  • Guo Y, Somerfield PJ, Warwick RM, Zhang Z (2001) Large-scale patterns in the community structure and biodiversity of free living nematodes in the Bohai Sea. China. J Mar Biol Ass UK 81:755–763

    Article  Google Scholar 

  • Hedfi A, Mahmoudi E, Boufahja F, Beyrem H, Aïssa P (2007) Effects of Increasing Levels of Nickel Contamination on Structure of Offshore Nematode Communities in Experimental Microcosms. Bull Environ Contam Toxicol 79:345–349

    Article  CAS  Google Scholar 

  • Ho NFH, Geary TG, Raub TJ, Barsuhn CL, Thompson DP (1990) Biophysical transport properties of the cuticle of Ascaris suum. Mol Biochem Parasitol 41(2):153–165

    Article  CAS  Google Scholar 

  • Jonker MTO (2008) Absorption of polycyclic aromatic hydrocarbons to cellulose. Chemosphere 70(5):778–782

    Article  CAS  Google Scholar 

  • Juario JV (1975) Nematodes species composition and seasonal fluctuation of sublittoral meiofauna community in the German Bight. Veröff Inst Meeresf Bremerhaven 15:283–337

    Google Scholar 

  • Louati H, Ben Said O, Soltani A, Got P, Mahmoudi E, Cravo-Laureau C, Duran R, Aissa P, Pringault O (2013) The roles of biological interactions and pollutant contamination in shaping microbial benthic community structure. Chemosphere 93(10):2535–2546

    Article  CAS  Google Scholar 

  • Louati H, Said OB, Soltani A, Got P, Cravo-Laureau C, Duran R, Aissa P, Pringault O, Mahmoudi E (2014) Biostimulation as an attractive technique to reduce phenanthrene toxicity for meiofauna and bacteria in lagoon sediment. Environ Sci Poll Res 21:3670–3679

    Article  CAS  Google Scholar 

  • Mahmoudi E, Essid N, Beyrem H, Hedfi A, Boufahja F, Vtiello P, Aissa P (2005) Effects of hydrocarbon contamination on a free living marine nematode community: Results from microcosm experiments. Mar Poll Bull 50:1197–1204

    Article  CAS  Google Scholar 

  • Massol F, Gravel D, Mouquet N, Cadotte MW, Fukami T, Leibold MA (2011) Linking community and ecosystem dynamics through spatial ecology. Ecol Lett 14:313–323

    Article  Google Scholar 

  • Moens T, Bouillon S, Gallucci F (2005) Dual stable isotope abundances unravel trophic position of estuarine nematodes. J Mar Biol Assoc UK 85:1401–1407

    Article  CAS  Google Scholar 

  • Moens T, Vincx M (1997) Observations on the feeding ecology of estuarine nematodes. J Mar Biol Assoc UK 77:211–227

    Article  Google Scholar 

  • Muir L, Lee YC (1970) Glycopeptides from earthworm cuticle collagen. J Biol Chem 245(3):502–509

    Article  CAS  Google Scholar 

  • Pathiratne A, Hemachandra CK, Pathiratne KAS (2010) Assessment of bile fluorescence patterns in a tropical fish, Nile Tilapia (Oreochromis niloticus) exposed to naphthalene, phenanthrene, pyrene and chrysene using fixed wavelength fluorescence and synchronous fluorescence spectrometry. Bull Environ Contam Toxicol 84:554–558

    Article  CAS  Google Scholar 

  • Platt HM, Warwick RM (1983) Free-living marine nematodes. Part I. British Enoploids. Cambridge University, London 307 p

  • Platt HM, Warwick RM (1988) Free-living marine nematodes. Part II. British Chromadorids. Synopsis of the British fauna (New Series). No. 38, E.J. Brill/W.Backhuys, Leiden

  • Pearson TH, Rosenberg R (1978) Macrobenthic Succession in Relation to Organic Enrichment and Pollution of the Marine Environment. Oceanogr Mar Biol 16:229–311

    Google Scholar 

  • Pellerone FI, Archer SK, Behm CA, Grant WN, Lacey MJ, Somerville AC (2003) Trehalose metabolism genes in Caenorhabditis elegans and filarial nematodes. Int J Parasitol 11:1195–1206

    Article  Google Scholar 

  • Riemann F, Schrage M (1978) The mucus-trap hypothesis on feeding of aquatic nematodes and implications for biodegradation and sediment texture. Oecologia 34:75–88

    Article  Google Scholar 

  • Reyzer ML, Caprioli RM (2007) MALDI-MS-based imaging of small molecules and proteins in tissues. Curr Opin Chem Biol 11:29–35

    Article  CAS  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    Article  CAS  Google Scholar 

  • Schratzberger M, Rees HL, Boyd SE (2000a) Effects of simulated deposition of dredged material on structure of nematode assemblages - the role of burial. Mar Biol 136:519–530

    Article  Google Scholar 

  • Schratzberger M, Rees HL, Boyd SE (2000b) Effects of simulated deposition of dredged material on structure of nematode assemblages - the role of contamination. Mar Biol 137:613–622

    Article  Google Scholar 

  • Schratzberger M, Whomersley P, Warr K, Bolam SG, Rees HL (2004) Colonisation of various types of sediment by estuarine nematodes via lateral infaunal migration: a laboratory study. Mar Biol 145:69–78

    Article  Google Scholar 

  • Seinhorst JW (1959) A rapid method for the transfer of nematodes from fixative to anhydrous glycerine. Nematologica 4:67–69

    Article  Google Scholar 

  • Sun M, Liu K, Zhao Y, Tian D, Ye M, Liu M, Jiao J, Jiang X (2017) Effects of Bacterial-Feeding Nematode Grazing and Tea Saponin Addition on the Enhanced Bioremediation of Pyrene-Contaminated Soil Using Polycyclic Aromatic Hydrocarbon-Degrading Bacterial Strain. Pedosphere 27(6):1062–1072

    Article  CAS  Google Scholar 

  • Takahashi K, Kozuka T, Anegawa A, Nagatani A, Mimura T (2015) Development and Application of a High-Resolution Imaging Mass Spectrometer for the Study of Plant Tissues. Plant Cell Physiol 56:1329–1338

    Article  CAS  Google Scholar 

  • Ukalska-Jaruga A, Smreczak B (2020) The Impact of Organic Matter on Polycyclic Aromatic Hydrocarbon (PAH) Availability and Persistence in Soils. Molecules 25(11):2470

    Article  CAS  Google Scholar 

  • Vitiello P, Dinet A (1979) Définition et échantillonnage du méiobenthos. Rapp Comm Int Mer Médit 25:279–283

    Google Scholar 

  • Wang P, Zhu Y, Lu H, Zhang Y (2010) Visualizing localizations and movement of anthracene in Kandelia candel (L.) Druce leaves by fluorescence microscopy. J Coast Res 26:549–554

    Article  Google Scholar 

  • Warwick RM, Platt HM, Somerfield PJ (1998) Free-living marine nematodes. Part III. ‎British monohysterids. Synopsis of British fauna (new series) No. 53, Field Studies ‎Council, Shrewsbury.‎ne nematodes

  • Warwick RM, Price R (1979) Ecological and metabolic studies on free-living nematodes from an estuarine mud-flat. Estuarine and Coastal Marine Science 9(3):257–271

    Article  Google Scholar 

  • Wieser W (1960) Benthic studies in Buzzards Bay. II. The meiofauna. Limnol Oceanogr 5:121–137

    Article  Google Scholar 

  • Wild E, Dent J, Barber JL, Thomas GO, Jones KC (2004) A novel analytical approach for visualizing and tracking organic chemicals in plants. Environ Sci Technol 38:4195–4199

    Article  CAS  Google Scholar 

  • Ye H, Gemperline E, Venkateshwaran M, Chen R, Delaux PM, Howes-Podoll M, Ané JM, Li L (2013) MALDI mass spectrometry-assisted molecular imaging of metabolites during nitrogen fixation in the Medicago truncatula-Sinorhizobium meliloti symbiosis. Plant J 75:130–145

    Article  CAS  Google Scholar 

  • Yin J, Ren W, Yang G, Duan J, Huang X, Fang R, Li C, Li T, Yin Y, Hou Y, Kim SW, Wu G (2016) L-Cysteine metabolism and its nutritional implications. Mol Nutr Food Res 60:134–146

    Article  CAS  Google Scholar 

  • Zhenjun S, Xianchun L, Lihui S, Chunyang S (1997) Earthworm as a potential protein resource. Ecol Food Nutr 36:221–236

    Article  Google Scholar 

  • Zhou H (2001) Effects of leaf litter addition on meiofaunal colonization of azoic sediments in a subtropical mangrove in Hong Kong. J Exp Mar Biol Ecol 256:99–121

    Article  CAS  Google Scholar 

  • Zrafi I, Safi N, Safi B, Mzoughi N, Aissi A, Ben Abdennebi H, Saidane D (2010) Distribution and Sources of Polycyclic Aromatic Hydrocarbons Around a Petroleum Refinery Rejection Area in Jarzouna-Bizerte (Coastal Tunisia). Soil Sediment Contam. 19:292–306

    Article  Google Scholar 

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Acknowledgments

The authors extendtheir appreciation to Researchers Supporting Project number RSP-2021/17, King Saud University, Riyadh, Saudi Arabia. The authors also thank Dr. Mateusz Płóciennik (University of Łódz, Poland) for the valuable assistance during the fluorescence examinations.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Funding

The authors extendtheir appreciation to Researchers Supporting Project number RSP-2021/17, King Saud University, Riyadh, Saudi Arabia.

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Mohamed Allouche: formal analysis, validation, writing (original draft), writing (review and editing). Ahmed Nasri: data curation, investigation. Abdel Halim Harrath: funding acquisition, writing (review and editing). Lamjed Mansour: funding acquisition, writing (review and editing). Saleh Alwasel: funding acquisition, investigation. Hamouda Beyrem: data curation, investigation. Gabriel Plăvan: investigation. Melissa Rohal-Lupher: writing (review and editing). Fehmi Boufahja: conceptualization, formal analysis, funding acquisition, investigation, methodology, supervision, validation, writing (review and editing).

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Correspondence to Fehmi Boufahja.

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Allouche, M., Nasri, A., Harrath, A.H. et al. Meiobenthic nematode Oncholaimus campylocercoides as a model in laboratory studies: selection, culture, and fluorescence microscopy after exposure to phenanthrene and chrysene. Environ Sci Pollut Res 28, 29484–29497 (2021). https://doi.org/10.1007/s11356-021-12688-1

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