[en] Antarctic specimens collected during various research expeditions are preserved in natural history collections around the world potentially offering a cornucopia of morphological and molecular data. Historical samples of marine species are, however, often preserved in formaldehyde which may render them useless for genetic analysis. We sampled stomachs and hindguts from 225 Trematomus specimens from the Natural History Museum London. These samples were initially collected between 20 and 100 years ago and fixed in either formaldehyde or ethanol. A 313 bp fragment of the cytochrome c oxidase subunit I (COI) was amplified and sequenced for prey item identification in the stomach and a 450 bp region of the 16S rRNA gene to investigate microbiome composition in the gut system. Both data sets were characterized by large dropout rates during extensive quality controls. Eventually, no unambiguous results regarding stomach content (COI) were retained, possibly due to degraded DNA, inefficient primers and contamination. In contrast, reliable microbiome composition data (16S rRNA) was obtained from 26 samples. These data showed a correlation in change of microbiome composition with fish size as well as year of the catch, indicating a microbiome shift throughout ontogeny and between samples from different decades. A comparison with contemporary samples indicated that the intestinal microbiome of Trematomus may have drastically changed within the last century. Further extensive studies are needed to confirm these patterns with higher sample numbers. Molecular analyses of museum stored fish can provide novel micro evolutionary insights that may benefit current efforts to prioritize conservation units in the Southern Ocean.
Research center :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Andrews S. (2010). FastQC: A Quality Control Tool for High Thoughout Sequence Data [Online]. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc (Accessed 10.6.2017).
Aylagas E. Rodríguez-Ezpeleta N. (2016). Analysis of illumina MiSeq metabarcoding data: application to benthic indices for environmental monitoring in Marine Genomics: Methods and Protocols, ed Bourlat S.J. (New York, NY: Springer New York), 237–249.
Bäckhed F. Ding H. Wang T. Hooper L. V. Koh G. Y. Nagy A. et al. (2004). The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. U. S. A. 101, 15718–15723. 10.1073/pnas.040707610115505215
Bagi A. Riiser E. S. Molland H. S. Star B. Haverkamp T. H. Sydnes M. O. et al. (2018). Gastrointestinal microbial community changes in Atlantic cod (Gadus morhua) exposed to crude oil. BMC Microbiol. 18:25. 10.1186/s12866-018-1171-229609542
Bellemain E. Davey M. L. Kauserud H. Epp L. S. Boessenkool S. Coissac E. et al. (2013). Fungal palaeodiversity revealed using high-throughput metabarcoding of ancient DNA from arctic permafrost. Environ. Microbiol. 15, 1176–1189. 10.1111/1462-2920.1202023171292
Bi K. Linderoth T. Vanderpool D. Good J. M. Nielsen R. Moritz C. (2013). Unlocking the vault: next-generation museum population genomics. Mol. Ecol. 22, 6018–6032. 10.1111/mec.1251624118668
Bi K. Vanderpool D. Singhal S. Linderoth T. Moritz C. Good J. M. (2012). Transcriptome-based exon capture enables highly cost-effective comparative genomic data collection at moderate evolutionary scales. BMC Genomics 13:403. 10.1186/1471-2164-13-40322900609
Bolger A. M. Lohse M. Usadel B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014, 2114–2120. 10.1093/bioinformatics/btu170
Brenner M. Buck B. H. Cordes S. Dietrich L. Jacob U. Mintenbeck K. et al. (2001). The role of iceberg scours in niche separation within the antarctic fish genus trematomus. Polar Biol. 24, 502–507. 10.1007/s003000100246
Caporaso J. G. Kuczynski J. Stombaugh J. Bittinger K. Bushman F. D. Costello E. K. et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336. 10.1038/nmeth.f.30320383131
Ceballos G. Ehrlich P. R. (2002). Mammal population losses and the extinction crisis. Science 296, 904–907. 10.1126/science.106934911988573
Chakraborty A. Sakai M. Iwatsuki Y. (2006). Museum fish specimens and molecular taxonomy: a comparative study on DNA extraction protocols and preservation techniques. J. Appl. Ichthyol. 22, 160–166. 10.1111/j.1439-0426.2006.00718.x
Chen L. Devries A. L. Cheng C.-H. C. (1997). Evolution of antifreeze glycoprotein gene from a trypsinogen gene in Antarctic notothenioid fish. Proc. Natl. Acad. Sci. 94, 3811–3816. 10.1073/pnas.94.8.38119108060
Chen L. Hu C. Lai N. L.-S. Zhang W. Hua J. Lam P. K. et al. (2018). Acute exposure to PBDEs at an environmentally realistic concentration causes abrupt changes in the gut microbiota and host health of zebrafish. Environ. Poll. 240, 17–26. 10.1016/j.envpol.2018.04.06229729565
Cho I. Blaser M. J. (2012). The human microbiome: at the interface of health and disease. Nat. Rev. Genet. 13:260. 10.1038/nrg318222411464
Clarke A. Harris C. M. (2003). Polar marine ecosystems: major threats and future change. Environ. Conserv. 30, 1–25. 10.1017/S0376892903000018
Cryan J. F. Dinan T. G. (2012). Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 13, 701–712. 10.1038/nrn334622968153
David L. A. Materna A. C. Friedman J. Campos-Baptista M. I. Blackburn M. C. Perrotta A. et al. (2014a). Host lifestyle affects human microbiota on daily timescales. Genome Biol. 15:R89. 10.1186/gb-2014-15-7-r8925146375
David L. A. Maurice C. F. Carmody R. N. Gootenberg D. B. Button J. E. Wolfe B. E. et al. (2014b). Diet rapidly and reproducibly alters the human gut microbiome. Nature 505:559. 10.1038/nature1282024336217
Dawson T. P. Jackson S. T. House J. I. Prentice I. C. Mace G. M. (2011). Beyond predictions: biodiversity conservation in a changing climate. science 332, 53–58. 10.1126/science.120030321454781
Deagle B. E. Jarman S. N. Coissac E. Pompanon F. Taberlet P. (2014). DNA metabarcoding and the cytochrome c oxidase subunit I marker: not a perfect match. Biol. Lett. 10:20140562. 10.1098/rsbl.2014.056225209199
Dewitt H. H. Heemstra P. C. Gon O. (1990). Nototheniidae: In Fishes of the Southern Ocean, eds Gon O. Heemstra P. C. Grahamstown: J.L.B. Smith Institute of Ichthyology.
Dornburg A. Federman S. Lamb A. D. Jones C. D. Near T. J. (2017). Cradles and museums of Antarctic teleost biodiversity. Nat. Ecol. Evol. 1:1379. 10.1038/s41559-017-0239-y29046532
Duhamel G. Hulley P.-A. Causse R. Koubbi P. Vacchi M. Pruvost P. et al. (2014). Biogeographic Patterns of Fish: in Biographic Atlas of the Southern Ocean. Cambridge: Scientific Committee on Antarctic Research.
Eastman J. T. (1993). Antarctic Fish Biology: Evolution in a Unique Environment. San Diego, CA: Academic Press.
Eastman J. T. Devries A. L. (1981). Buoyancy adaptations in a swim-bladderless Antarctic fish. J. Morphol. 167, 91–102. 10.1002/jmor.105167010830111003
Edgar R. C. Haas B. J. Clemente J. C. Quince C. Knight R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200. 10.1093/bioinformatics/btr38121700674
Egerton S. Culloty S. Whooley J. Stanton C. Ross R. P. (2018). The gut microbiota of marine fish. Front. Microbiol. 9:00873. 10.3389/fmicb.2018.0087329780377
Eisenhofer R. Anderson A. Dobney K. Cooper A. Weyrich L. S. (2017). Ancient microbial DNA in dental calculus: a new method for studying rapid human migration events. J. Island Coast. Archaeol. 2017, 1–14. 10.1080/15564894.2017.1382620
El Aidy S. Van Baarlen P. Derrien M. Lindenbergh-Kortleve D. J. Hooiveld G. Levenez F. et al. (2012). Temporal and spatial interplay of microbiota and intestinal mucosa drive establishment of immune homeostasis in conventionalized mice. Mucosal Immunol. 5:567. 10.1038/mi.2012.3222617837
El Aidy S. Van Den Abbeele P. Van De Wiele T. Louis P. Kleerebezem M. (2013). Intestinal colonization: how key microbial players become established in this dynamic process. Bioessays 35, 913–923. 10.1002/bies.20130007323946088
Ficetola G. F. Taberlet P. Coissac E. (2016). How to limit false positives in environmental DNA and metabarcoding? Mol. Ecol. Resour. 16, 604–607. 10.1111/1755-0998.1250827062589
Funkhouser L. J. Bordenstein S. R. (2013). Mom knows best: the universality of maternal microbial transmission. PLoS Biol. 11:e1001631. 10.1371/journal.pbio.100163123976878
Geiduschek E. P. (1958). On the reversibility of the acid denaturation of sodium desoxyribose nucleate. J. Polymer Sci. Part A 31, 67–75.
Ghanbari M. Kneifel W. Domig K. J. (2015). A new view of the fish gut microbiome: advances from next-generation sequencing. Aquaculture 448, 464–475. 10.1016/j.aquaculture.2015.06.033
Griffiths H. J. Meijers A. J. Bracegirdle T. J. (2017). More losers than winners in a century of future Southern Ocean seafloor warming. Nat. Clim. Chang. 7, 749. 10.1038/nclimate3377
Halpern B. S. Walbridge S. Selkoe K. A. Kappel C. V. Micheli F. D'agrosa C. et al. (2008). A global map of human impact on marine ecosystems. Science 319, 948–952. 10.1126/science.114934518276889
Herbin M. (2013). La conservation des collections en fluide. CeROArt 259. Available Online at: http://journals.openedition.org/ceroart/3432
Higuchi R. Bowman B. Freiberger M. Ryder O. A. Wilson A. C. (1984). DNA sequences from the quagga, an extinct member of the horse family. Nature 312, 282–284. 10.1038/312282a06504142
Hofmann G. E. Buckley B. A. Airaksinen S. Keen J. E. Somero G. N. (2000). Heat-shock protein expression is absent in the antarctic fish Trematomus bernacchii (family Nototheniidae). J. Exp. Biol. 203, 2331–2339.10887071
Janko K. Marshall C. Musilov,á Z. Van Houdt J. Couloux A. Cruaud C. et al. (2011). Multilocus analyses of an Antarctic fish species flock (Teleostei, Notothenioidei, Trematominae): phylogenetic approach and test of the early-radiation event. Mol. Phylogenet. Evol. 60, 305–316. 10.1016/j.ympev.2011.03.00821402163
Jørgensen T. Kjær K. H. Haile J. Rasmussen M. Boessenkool S. Andersen K. et al. (2012). Islands in the ice: detecting past vegetation on Greenlandic nunataks using historical records and sedimentary ancient DNA Meta-barcoding. Mol. Ecol. 21, 1980–1988. 10.1111/j.1365-294X.2011.05278.x21951625
Joshi B. D. Mishra S. Singh S. K. Goyal S. (2013). An effective method for extraction and polymerase chain reaction (PCR) amplification of DNA from formalin preserved tissue samples of snow leopard. Afr. J. Biotechnol. 12, 3399–3404. 10.5897/AJB12.2759
Jurajda P. Roche K. Sedláček I. Všetičkov,á L. (2016). Assemblage characteristics and diet of fish in the shallow coastal waters of James Ross Island, Antarctica. Polar Biol. 39, 1–11. 10.1007/s00300-016-1896-z
Kau A. L. Ahern P. P. Griffin N. W. Goodman A. L. Gordon J. I. (2011). Human nutrition, the gut microbiome and the immune system. Nature 474, 327–336. 10.1038/nature1021321677749
Klindworth A. Pruesse E. Schweer T. Peplies J. Quast C. Horn M. et al. (2013). Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 41:e1. 10.1093/nar/gks80822933715
Koshiba M. Ogawa K. Hamazaki S. Sugiyama T. Ogawa O. Kitajima T. (1993). The effect of formalin fixation on DNA and the extraction of high-molecular-weight DNA from fixed and embedded tissues. Pathol. Res. Pract. 189, 66–72. 10.1016/S0344-0338(11)80118-48390645
La Mesa M. Catalano B. Jones C. D. (2015). Early life history traits of Trematomus scotti in the Bransfield Strait. Antarctic Sci. 27, 535–542. 10.1017/S0954102015000280
La Mesa M. Dal,ú M. Vacchi M. (2004). Trophic ecology of the emerald notothen Trematomus bernacchii (pisces, nototheniidae) from Terra Nova Bay, Ross Sea, Antarctica. Polar Biol. 27, 721–728. 10.1007/s00300-004-0645-x
La Mesa M. Vacchi M. Castelli A. Diviacco G. (1997). Feeding ecology of two nototheniid fishes, Trematomus hansoni and Trematomus loennbergii, from Terra Nova Bay, Ross Sea. Polar Biol. 17, 62–68. 10.1007/s003000050105
Lambert D. Ritchie P. Millar C. Holland B. Drummond A. Baroni C. (2002). Rates of evolution in ancient DNA from Adélie penguins. Science 295, 2270–2273. 10.1126/science.106810511910113
Lange V. Böhme I. Hofmann J. Lang K. Sauter J. Schöne B. et al. (2014). Cost-efficient high-throughput HLA typing by MiSeq amplicon sequencing. BMC Genom. 15:63. 10.1186/1471-2164-15-6324460756
Lannoo M. J. Eastman J. T. (2000). Nervous and sensory system correlates of an epibenthic evolutionary radiation in Antarctic notothenioid fishes, genus Trematomus (Perciformes; Nototheniidae). J. Morphol. 245, 67–79. 10.0.3.234/1097-4687(200007)245:1%3C67::AID-JMOR5%3E3.0.CO;2-W10861832
Leray M. Yang J. Y. Meyer C. P. Mills S. C. Agudelo N. Ranwez V. et al. (2013). A new versatile primer set targeting a short fragment of the mitochondrial COI region for metabarcoding metazoan diversity: application for characterizing coral reef fish gut contents. Front. Zool. 10:34. 10.1186/1742-9994-10-3423767809
Lundvall D. Svanbäck R. Persson L. Byström P. (1999). Size-dependent predation in piscivores: interactions between predator foraging and prey avoidance abilities. Canad. J. Fish. Aquat. Sci. 56, 1285–1292. 10.1139/f99-058
Magoč T. Salzberg S. L. (2011). FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963. 10.1093/bioinformatics/btr50721903629
Matschiner M. Hanel R. Salzburger W. (2011). On the origin and trigger of the notothenioid adaptive radiation. PLoS ONE 6:e18911. 10.1371/journal.pone.001891121533117
Mcmullin R. M. Wing S. R. Wing L. C. Shatova O. A. (2017). Trophic position of Antarctic ice fishes reflects food web structure along a gradient in sea ice persistence. Mar. Ecol. Prog. Ser. 564, 87–98. 10.3354/meps12031
Mintenbeck K. Barrera-Oro E. R. Brey T. Jacob U. Knust R. Mark F. C. et al. (2012). Impact of climate change on fishes in complex antarctic ecosystems. Adv. Ecol. Res. 46, 351–426. 10.1016/B978-0-12-396992-7.00006-X
Moreira E. Juáres M. Barrera-Oro E. (2014). Dietary overlap among early juvenile stages in an Antarctic notothenioid fish assemblage at Potter Cove, South Shetland Islands. Polar Biol. 37, 1507–1515. 10.1007/s00300-014-1545-3
Near T. J. Dornburg A. Kuhn K. L. Eastman J. T. Pennington J. N. Patarnello T. et al. (2012). Ancient climate change, antifreeze, and the evolutionary diversification of Antarctic fishes. Proc. Natl. Acad. Sci. 109, 3434–3439. 10.1073/pnas.111516910922331888
NEPHELE (2016). Office of Cyber Infrastructure and Computational Biology (OCICB), National Institute of Allergy and Infectious Diseases (NIAID). Nephele. [Online]. Available online at: http://nephele.niaid.nih.gov (Accessed 01-04 2018).
Nielsen E. E. Morgan J. Maher S. Edson J. Gauthier M. Pepperell J. et al. (2017). Extracting DNA from ‘jaws': high yield and quality from archived tiger shark (Galeocerdo cuvier) skeletal material. Mol. Ecol. Resour. 17, 431–442. 10.1111/1755-0998.1258027508520
Porter T. M. Hajibabaei M. (2018). Scaling up: a guide to high-throughput genomic approaches for biodiversity analysis. Mol. Ecol. 27, 313–338. 10.1111/mec.1447829292539
Postlethwait J. H. Yan Y. L. Desvignes T. Allard C. Titus T. Le François N. R. et al. (2016). Embryogenesis and early skeletogenesis in the antarctic bullhead notothen, Notothenia coriiceps. Dev. Dyn. 245, 1066–1080. 10.1002/dvdy.2443727507212
Quast C. Pruesse E. Yilmaz P. Gerken J. Schweer T. Yarza P. et al. (2012). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596. 10.1093/nar/gks,121923193283
R Core Team (2016). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. Available online at: https://www.R-project.org/
Roessig J. M. Woodley C. M. Cech J. J. Hansen L. J. (2004). Effects of global climate change on marine and estuarine fishes and fisheries. Rev. Fish Biol. Fish 14, 251–275. 10.1007/s11160-004-6749-0
Romero J. Navarrete P. (2006). 16S rDNA-based analysis of dominant bacterial populations associated with early life stages of coho salmon (Oncorhynchus kisutch). Microb. Ecol. 51, 422–430. 10.1007/s00248-006-9037-9
Rutschmann S. Matschiner M. Damerau M. Muschick M. Lehmann M. F. Hanel R. et al. (2011). Parallel ecological diversification in Antarctic notothenioid fishes as evidence for adaptive radiation. Mol. Ecol. 20, 4707–4721. 10.1111/j.1365-294X.2011.05279.x21951675
Sato Y. Sugie R. Tsuchiya B. Kameya T. Natori M. Mukai K. (2001). Comparison of the DNA extraction methods for polymerase chain reaction amplification from formalin-fixed and paraffin-embedded tissues. Diagn. Mol. Pathol. 10, 265–271. 10.1097/00019606-200112000-0000911763318
Schloss P. D. Westcott S. L. Ryabin T. Hall J. R. Hartmann M. Hollister E. B. et al. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–7541. 10.1128/AEM.01541-0919801464
Schnorr S. L. Sankaranarayanan K. Lewis C. M. Warinner C. (2016). Insights into human evolution from ancient and contemporary microbiome studies. Curr. Opin. Genet. Dev. 41, 14–26. 10.1016/j.gde.2016.07.00327507098
Schofield O. Ducklow H. W. Martinson D. G. Meredith M. P. Moline M. A. Fraser W. R. (2010). How do polar marine ecosystems respond to rapid climate change? Science 328, 1520–1523. 10.1126/science.118577920558708
Shi S.-R. Cote R. J. Wu L. Liu C. Datar R. Shi Y. et al. (2002). DNA extraction from archival formalin-fixed, paraffin-embedded tissue sections based on the antigen retrieval principle: heating under the influence of pH. J. Histochem. Cytochem. 50, 1005–1011. 10.1177/00221554020500080212133903
Shi S.-R. Datar R. Liu C. Wu L. Zhang Z. Cote R. J. et al. (2004). DNA extraction from archival formalin-fixed, paraffin-embedded tissues: heat-induced retrieval in alkaline solution. Histochem. Cell Biol. 122, 211–218. 10.1007/s00418-004-0693-x15322858
Solomon S. Plattner G.-K. Knutti R. Friedlingstein P. (2009). Irreversible climate change due to carbon dioxide emissions. Proc. Natl. Acad. Sci. 106, 1704–1709. 10.1073/pnas.081272110619179281
Sullam K. E. Essinger S. D. Lozupone C. A. O'connor M. P. Rosen G. L. Knight R. et al. (2012). Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis. Mol. Ecol. 21, 3363–3378. 10.1111/j.1365-294X.2012.05552.x22486918
Tarnecki A. M. Burgos F. A. Ray C. L. Arias C. R. (2017). Fish intestinal microbiome: diversity and symbiosis unraveled by metagenomics. J. Appl. Microbiol. 7, 2–17. 10.1111/jam.13415
Thomas C. A. Doty P. (1956). The mild acidic degradation of desoxyribose nucleic acid. J. Am. Chem. Soc. 78, 1854–1860. 10.1021/ja01590a023
Tito R. Y. Knights D. Metcalf J. Obregon-Tito A. J. Cleeland L. Najar F. et al. (2012). Insights from characterizing extinct human gut microbiomes. PLoS ONE 7, e51146. 10.1371/journal.pone.005114623251439
Trathan P. N. Agnew D. (2010). Climate change and the Antarctic marine ecosystem: an essay on management implications. Antarctic Sci. 22, 387–398. 10.1017/S0954102010000222
Turnbaugh P. J. Ley R. E. Mahowald M. A. Magrini V. Mardis E. R. Gordon J. I. (2006). An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027–1131. 10.1038/nature0541417183312
Vacchi M. La Mesa M. (1995). The diet of the Antarctic fish Trematomus newnesi Boulenger, 1902 (Nototheniidae) from Terra Nova Bay, Ross Sea. Antarctic Sci. 7, 37–38. 10.1017/S0954102095000071
Van De Putte A. P. Janko K. Kasparova E. Maes G. E. Rock J. Koubbi P. et al. (2012). Comparative phylogeography of three trematomid fishes reveals contrasting genetic structure patterns in benthic and pelagic species. Mar. Genom. 8, 23–34. 10.1016/j.margen.2012.05.00223199877
Wandeler P. Hoeck P. E. Keller L. F. (2007). Back to the future: museum specimens in population genetics. Trends Ecol. Evol. 22, 634–642. 10.1016/j.tree.2007.08.01717988758
Ward N. L. Steven B. Penn K. Meth,é B. A. Detrich W. H. (2009). Characterization of the intestinal microbiota of two Antarctic notothenioid fish species. Extremophiles 13, 679–685. 10.1007/s00792-009-0252-419472032
White M. (1991). Age determination in Antarctic fish in Biology of Antarctic fish. eds. di Prisco G. Maresca B. Tota B. (Berlin: Springer), 87–100.
Willerslev E. Davison J. Moora M. Zobel M. Coissac E. Edwards M. E. et al. (2014). Fifty thousand years of Arctic vegetation and megafaunal diet. Nature 506:47. 10.1038/nature1292124499916
Zakrzewski M. Proietti C. Ellis J. J. Hasan S. Brion M.-J. Berger B. et al. (2016). Calypso: a user-friendly web-server for mining and visualizing microbiome–environment interactions. Bioinformatics 33, 782–283. 10.1093/bioinformatics/btw72528025202