Identifying the plant‐associated microbiome across aquatic and terrestrial environments: the effects of amplification method on taxa discovery
Plants in terrestrial and aquatic environments contain a diverse microbiome. Yet, the chloroplast and mitochondria organelles of the plant eukaryotic cell originate from free‐living cyanobacteria and Rickettsiales. This represents a challenge for sequencing the plant microbiome with universal primer...
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Freeman
2017
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Online Access: | https://hdl.handle.net/2027.42/138887 https://doi.org/10.1111/1755-0998.12645 |
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ftumdeepblue:oai:deepblue.lib.umich.edu:2027.42/138887 |
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Open Polar |
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University of Michigan: Deep Blue |
op_collection_id |
ftumdeepblue |
language |
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topic |
plant microbiome Proteobacteria aquatic environments PNA clamps Earth microbiome project chloroplast Ecology and Evolutionary Biology Science |
spellingShingle |
plant microbiome Proteobacteria aquatic environments PNA clamps Earth microbiome project chloroplast Ecology and Evolutionary Biology Science Jackrel, Sara L. Owens, Sarah M. Gilbert, Jack A. Pfister, Catherine A. Identifying the plant‐associated microbiome across aquatic and terrestrial environments: the effects of amplification method on taxa discovery |
topic_facet |
plant microbiome Proteobacteria aquatic environments PNA clamps Earth microbiome project chloroplast Ecology and Evolutionary Biology Science |
description |
Plants in terrestrial and aquatic environments contain a diverse microbiome. Yet, the chloroplast and mitochondria organelles of the plant eukaryotic cell originate from free‐living cyanobacteria and Rickettsiales. This represents a challenge for sequencing the plant microbiome with universal primers, as ~99% of 16S rRNA sequences may consist of chloroplast and mitochondrial sequences. Peptide nucleic acid clamps offer a potential solution by blocking amplification of host‐associated sequences. We assessed the efficacy of chloroplast and mitochondria‐blocking clamps against a range of microbial taxa from soil, freshwater and marine environments. While we found that the mitochondrial blocking clamps appear to be a robust method for assessing animal‐associated microbiota, Proteobacterial 16S rRNA binds to the chloroplast‐blocking clamp, resulting in a strong sequencing bias against this group. We attribute this bias to a conserved 14‐bp sequence in the Proteobacteria that matches the 17‐bp chloroplast‐blocking clamp sequence. By scanning the Greengenes database, we provide a reference list of nearly 1500 taxa that contain this 14‐bp sequence, including 48 families such as the Rhodobacteraceae, Phyllobacteriaceae, Rhizobiaceae, Kiloniellaceae and Caulobacteraceae. To determine where these taxa are found in nature, we mapped this taxa reference list against the Earth Microbiome Project database. These taxa are abundant in a variety of environments, particularly aquatic and semiaquatic freshwater and marine habitats. To facilitate informed decisions on effective use of organelle‐blocking clamps, we provide a searchable database of microbial taxa in the Greengenes and Silva databases matching various n‐mer oligonucleotides of each PNA sequence. Peer Reviewed https://deepblue.lib.umich.edu/bitstream/2027.42/138887/1/men12645.pdf https://deepblue.lib.umich.edu/bitstream/2027.42/138887/2/men12645_am.pdf https://deepblue.lib.umich.edu/bitstream/2027.42/138887/3/men12645-sup-0001-SupInfo.pdf |
format |
Article in Journal/Newspaper |
author |
Jackrel, Sara L. Owens, Sarah M. Gilbert, Jack A. Pfister, Catherine A. |
author_facet |
Jackrel, Sara L. Owens, Sarah M. Gilbert, Jack A. Pfister, Catherine A. |
author_sort |
Jackrel, Sara L. |
title |
Identifying the plant‐associated microbiome across aquatic and terrestrial environments: the effects of amplification method on taxa discovery |
title_short |
Identifying the plant‐associated microbiome across aquatic and terrestrial environments: the effects of amplification method on taxa discovery |
title_full |
Identifying the plant‐associated microbiome across aquatic and terrestrial environments: the effects of amplification method on taxa discovery |
title_fullStr |
Identifying the plant‐associated microbiome across aquatic and terrestrial environments: the effects of amplification method on taxa discovery |
title_full_unstemmed |
Identifying the plant‐associated microbiome across aquatic and terrestrial environments: the effects of amplification method on taxa discovery |
title_sort |
identifying the plant‐associated microbiome across aquatic and terrestrial environments: the effects of amplification method on taxa discovery |
publisher |
Freeman |
publishDate |
2017 |
url |
https://hdl.handle.net/2027.42/138887 https://doi.org/10.1111/1755-0998.12645 |
genre |
Arctic |
genre_facet |
Arctic |
op_relation |
Jackrel, Sara L.; Owens, Sarah M.; Gilbert, Jack A.; Pfister, Catherine A. (2017). "Identifying the plant‐associated microbiome across aquatic and terrestrial environments: the effects of amplification method on taxa discovery." Molecular Ecology Resources 17(5): 931-942. 1755-098X 1755-0998 https://hdl.handle.net/2027.42/138887 doi:10.1111/1755-0998.12645 Molecular Ecology Resources Pfister CA, Altabet MA, Post D ( 2014 ) Animal regeneration and microbial retention of nitrogen along coastal rocky shores. Ecology, 95, 2803 – 2814. Jackrel SL, Morton TC, Wootton JT ( 2016 ) Intraspecific leaf chemistry drives locally accelerated ecosystem function in aquatic and terrestrial communities. Ecology, 97, 2125 – 2135. Kardol P, Cornips NJ, van Kempen MML, Bakx‐Schotman JMT, van der Putten WH ( 2007 ) Microbe‐mediated plant‐soil feedback causes historical contigency effects in plant community assembly. Ecological Monographs, 77, 147 – 162. Karkare S, Bhatnagar D ( 2006 ) Promising nucleic acid analogs and mimics: characteristic features and applications of PNA, LNA, and morpholino. Applied Microbiology and Biotechnology, 71, 575 – 586. Kwong WK, Moran NA ( 2016 ) Gut microbial communities of social bees. Nature Reviews Microbiology, 14, 374 – 384. Locey KJ, Lennon JT ( 2016 ) Scaling laws predict global microbial diversity. Proceedings of the National Academy of Sciences, 113, 5970 – 5975. Lundberg DS, Lebeis SL, Paredes SH et al. ( 2012 ) Defining the core Arabidopsis thaliana root microbiome. Nature, 488, 86 – 90. Lundberg DS, Yourstone S, Mieczkowski P, Jones CD, Dangl JL ( 2013 ) Practical innovations for high‐throughput amplicon sequencing. Nature Methods, 10, 999 – 1002. Margulis L ( 1981 ) Symbiosis in Cell Evolution: Life and its Environment on the Early Earth. Freeman, San Francisco. Muegge BD, Kuczynski J, Knights D et al. ( 2011 ) Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science, 332, 970 – 974. Mullis K. B., Erlich H. A., Arnheim N., Horn G. T., Saiki R. K., Scharf S. J. ( 1989 ). Process for Amplifying, Detecting, and/or Cloning Nucleic Acid Sequences. U.S. Patent 4683195 A Ørum H, Nielsen PE, Egholm M, Berg RH, Buchardt O, Stanley C ( 1993 ) Single base pair mutation analysis by PNA directed PCR clamping. Nucleic Acids Research, 21, 5332 – 5336. R Core Team ( 2013 ). R version 3: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Australia. www.r-project.org. Ray A, Nordén B ( 2000 ) Peptide nucleic acid (PNA): its medical and biotechnical applications and promise for the future. The FASEB Journal, 14, 1041 – 1060. Schloss PD, Westcott SL, Ryabin T et al. ( 2009 ) Introducing mothur: open‐source, platform‐independent, community‐supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75, 7537 – 7541. Shogan BD, Smith DP, Christley S, Gilbert JA, Zaborina O, Alverdy JC ( 2014 ) Intestinal anastomotic injury alters spatially defined microbiome composition and function. Microbiome, 2, 1 – 10. Sim K, Cox MJ, Wopereis H et al. ( 2012 ) Improved detection of bifidobacteria with optimised 16S rRNA‐gene based pyrosequencing. PLoS ONE, 7, e32543. Singh RP, Reddy CRK ( 2015 ) Unraveling the functions of the macroalgal microbiome. Frontiers in Microbiology, 6, 1488. Smith CCR, Snowberg LK, Gregory Caporaso J, Knight R, Bolnick DI ( 2015 ) Dietary input of microbes and host genetic variation shape among‐population differences in stickleback gut microbiota. ISME Journal, 9, 2515 – 2526. Sullam KE, Essinger SD, Lozupone CA et al. ( 2012 ) Environmental and ecological factors that shape the gut bacterial communities of fish: a meta‐analysis. Molecular Ecology, 21, 3363 – 3378. Taylor JD, Cottingham SD, Billinge J, Cunliffe M ( 2014 ) Seasonal microbial community dynamics correlate with phytoplankton‐derived polysaccharides in surface coastal waters. ISME Journal, 8, 245 – 248. Von Wintzingerode F, Landt O, Ehrlich A, Göbel UB ( 2000 ) Peptide nucleic‐acid mediated PCR clamping as a useful supplement in the determination of microbial diversity. Applied and Environmental Microbiology, 66, 549 – 557. Zak DR, Holmes WE, White DC, Peacock AD, Tilman D ( 2003 ) Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology, 84, 2042 – 2050. Zarraonaindia I, Owens SM, Weisenhorn P et al. ( 2015 ) The soil microbiome influences grapevine‐associated microbiota. mBio, 6, e02527 – 14. Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM ( 2013 ) Application of natural blends of phytochemicals derived from the root exudates of arabidopsis to the soil reveal that phenolic‐related compounds predominantly modulate the soil microbiome. Journal of Biological Chemistry, 288, 4502 – 4512. Benjamini Y, Hochberg Y ( 1995 ) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, 57, 289 – 300. Berendsen RL, Pieterse CMJ, Bakker PAHM ( 2012 ) The rhizosphere microbiome and plant health. Trends in Plant Science, 17, 478 – 486. Bolnick DI, Snowberg LK, Hirsch PE et al. ( 2014 ) Individual diet has sex‐dependent effects on vertebrate gut microbiota. Nature Communications, 5, 1 – 13. Campbell AH, Marzinelli EM, Gelber J, Steinberg PD ( 2015 ) Spatial variability of microbial assemblages associated with a dominant habitat‐forming seaweed. Frontiers in Microbiology, 6, 230. Caporaso JG, Kuczynski J, Stombaugh J et al. ( 2010 ) qiime allows analysis of high‐throughput community sequencing data. Nature Methods, 7, 335 – 336. Caporaso JG, Lauber CL, Walters WA et al. ( 2012 ) Ultra‐high‐throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME Journal, 6, 1621 – 1624. Chelius MK, Triplett EW ( 2001 ) The diversity of archaea and bacteria in association with the roots of Zea mays. Microbial Ecology, 41, 252 – 263. De Filippis F, Genovese A, Ferranti P, Gilbert JA, Ercolini D ( 2016 ) Metatranscriptomics reveals temperature‐driven functional changes in microbiome impacting cheese maturation rate. Scientific Reports, 6, 21871. Egan S, Harder T, Burke C, Steinberg P, Kjelleberg S, Thomas T ( 2013 ) The seaweed holobiont: understanding seaweed–bacteria interactions. FEMS Microbiology Reviews, 37, 462 – 476. Egholm M, Buchardt O, Christensen L et al. ( 1993 ) PNA hybridizes to complementary oligonucleotides obeying the Watson‐Crick hydrogen‐bonding rules. Nature, 365, 566 – 8. Fu Y, Keats KF, Rivkin RB, Lang AS ( 2013 ) Water mass and depth determine the distribution and diversity of Rhodobacterales in an Arctic marine system. FEMS Microbiology Ecology, 84, 564 – 576. Gilbert JA, Steele JA, Caporaso JG et al. ( 2012 ) Defining seasonal marine microbial community dynamics. ISME Journal, 6, 298 – 308. Gilbert JA, Jansson JK, Knight R ( 2014 ) The Earth Microbiome project: successes and aspirations. BMC Biology, 12, 1 – 4. Gower JC ( 1975 ) Generalized procrustes analysis. Psychometrika, 40, 33 – 51. Hanshew AS, Mason CJ, Raffa KF, Currie CR ( 2013 ) Minimization of chloroplast contamination in 16S rRNA gene pyrosequencing of insect herbivore bacterial communities. Journal of Microbiological Methods, 95, 149 – 155. Jackrel SL, Wootton JT ( 2014 ) Local adaptation of stream communities to intraspecific variation in a terrestrial ecosystem subsidy. Ecology, 95, 37 – 43. |
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ftumdeepblue:oai:deepblue.lib.umich.edu:2027.42/138887 2023-08-20T04:03:11+02:00 Identifying the plant‐associated microbiome across aquatic and terrestrial environments: the effects of amplification method on taxa discovery Jackrel, Sara L. Owens, Sarah M. Gilbert, Jack A. Pfister, Catherine A. 2017-09 application/pdf https://hdl.handle.net/2027.42/138887 https://doi.org/10.1111/1755-0998.12645 unknown Freeman Wiley Periodicals, Inc. Jackrel, Sara L.; Owens, Sarah M.; Gilbert, Jack A.; Pfister, Catherine A. (2017). "Identifying the plant‐associated microbiome across aquatic and terrestrial environments: the effects of amplification method on taxa discovery." Molecular Ecology Resources 17(5): 931-942. 1755-098X 1755-0998 https://hdl.handle.net/2027.42/138887 doi:10.1111/1755-0998.12645 Molecular Ecology Resources Pfister CA, Altabet MA, Post D ( 2014 ) Animal regeneration and microbial retention of nitrogen along coastal rocky shores. Ecology, 95, 2803 – 2814. Jackrel SL, Morton TC, Wootton JT ( 2016 ) Intraspecific leaf chemistry drives locally accelerated ecosystem function in aquatic and terrestrial communities. Ecology, 97, 2125 – 2135. Kardol P, Cornips NJ, van Kempen MML, Bakx‐Schotman JMT, van der Putten WH ( 2007 ) Microbe‐mediated plant‐soil feedback causes historical contigency effects in plant community assembly. Ecological Monographs, 77, 147 – 162. Karkare S, Bhatnagar D ( 2006 ) Promising nucleic acid analogs and mimics: characteristic features and applications of PNA, LNA, and morpholino. Applied Microbiology and Biotechnology, 71, 575 – 586. Kwong WK, Moran NA ( 2016 ) Gut microbial communities of social bees. Nature Reviews Microbiology, 14, 374 – 384. Locey KJ, Lennon JT ( 2016 ) Scaling laws predict global microbial diversity. Proceedings of the National Academy of Sciences, 113, 5970 – 5975. Lundberg DS, Lebeis SL, Paredes SH et al. ( 2012 ) Defining the core Arabidopsis thaliana root microbiome. Nature, 488, 86 – 90. Lundberg DS, Yourstone S, Mieczkowski P, Jones CD, Dangl JL ( 2013 ) Practical innovations for high‐throughput amplicon sequencing. Nature Methods, 10, 999 – 1002. Margulis L ( 1981 ) Symbiosis in Cell Evolution: Life and its Environment on the Early Earth. Freeman, San Francisco. Muegge BD, Kuczynski J, Knights D et al. ( 2011 ) Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science, 332, 970 – 974. Mullis K. B., Erlich H. A., Arnheim N., Horn G. T., Saiki R. K., Scharf S. J. ( 1989 ). Process for Amplifying, Detecting, and/or Cloning Nucleic Acid Sequences. U.S. Patent 4683195 A Ørum H, Nielsen PE, Egholm M, Berg RH, Buchardt O, Stanley C ( 1993 ) Single base pair mutation analysis by PNA directed PCR clamping. Nucleic Acids Research, 21, 5332 – 5336. R Core Team ( 2013 ). R version 3: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Australia. www.r-project.org. Ray A, Nordén B ( 2000 ) Peptide nucleic acid (PNA): its medical and biotechnical applications and promise for the future. The FASEB Journal, 14, 1041 – 1060. Schloss PD, Westcott SL, Ryabin T et al. ( 2009 ) Introducing mothur: open‐source, platform‐independent, community‐supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75, 7537 – 7541. Shogan BD, Smith DP, Christley S, Gilbert JA, Zaborina O, Alverdy JC ( 2014 ) Intestinal anastomotic injury alters spatially defined microbiome composition and function. Microbiome, 2, 1 – 10. Sim K, Cox MJ, Wopereis H et al. ( 2012 ) Improved detection of bifidobacteria with optimised 16S rRNA‐gene based pyrosequencing. PLoS ONE, 7, e32543. Singh RP, Reddy CRK ( 2015 ) Unraveling the functions of the macroalgal microbiome. Frontiers in Microbiology, 6, 1488. Smith CCR, Snowberg LK, Gregory Caporaso J, Knight R, Bolnick DI ( 2015 ) Dietary input of microbes and host genetic variation shape among‐population differences in stickleback gut microbiota. ISME Journal, 9, 2515 – 2526. Sullam KE, Essinger SD, Lozupone CA et al. ( 2012 ) Environmental and ecological factors that shape the gut bacterial communities of fish: a meta‐analysis. Molecular Ecology, 21, 3363 – 3378. Taylor JD, Cottingham SD, Billinge J, Cunliffe M ( 2014 ) Seasonal microbial community dynamics correlate with phytoplankton‐derived polysaccharides in surface coastal waters. ISME Journal, 8, 245 – 248. Von Wintzingerode F, Landt O, Ehrlich A, Göbel UB ( 2000 ) Peptide nucleic‐acid mediated PCR clamping as a useful supplement in the determination of microbial diversity. Applied and Environmental Microbiology, 66, 549 – 557. Zak DR, Holmes WE, White DC, Peacock AD, Tilman D ( 2003 ) Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology, 84, 2042 – 2050. Zarraonaindia I, Owens SM, Weisenhorn P et al. ( 2015 ) The soil microbiome influences grapevine‐associated microbiota. mBio, 6, e02527 – 14. Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM ( 2013 ) Application of natural blends of phytochemicals derived from the root exudates of arabidopsis to the soil reveal that phenolic‐related compounds predominantly modulate the soil microbiome. Journal of Biological Chemistry, 288, 4502 – 4512. Benjamini Y, Hochberg Y ( 1995 ) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, 57, 289 – 300. Berendsen RL, Pieterse CMJ, Bakker PAHM ( 2012 ) The rhizosphere microbiome and plant health. Trends in Plant Science, 17, 478 – 486. Bolnick DI, Snowberg LK, Hirsch PE et al. ( 2014 ) Individual diet has sex‐dependent effects on vertebrate gut microbiota. Nature Communications, 5, 1 – 13. Campbell AH, Marzinelli EM, Gelber J, Steinberg PD ( 2015 ) Spatial variability of microbial assemblages associated with a dominant habitat‐forming seaweed. Frontiers in Microbiology, 6, 230. Caporaso JG, Kuczynski J, Stombaugh J et al. ( 2010 ) qiime allows analysis of high‐throughput community sequencing data. Nature Methods, 7, 335 – 336. Caporaso JG, Lauber CL, Walters WA et al. ( 2012 ) Ultra‐high‐throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME Journal, 6, 1621 – 1624. Chelius MK, Triplett EW ( 2001 ) The diversity of archaea and bacteria in association with the roots of Zea mays. Microbial Ecology, 41, 252 – 263. De Filippis F, Genovese A, Ferranti P, Gilbert JA, Ercolini D ( 2016 ) Metatranscriptomics reveals temperature‐driven functional changes in microbiome impacting cheese maturation rate. Scientific Reports, 6, 21871. Egan S, Harder T, Burke C, Steinberg P, Kjelleberg S, Thomas T ( 2013 ) The seaweed holobiont: understanding seaweed–bacteria interactions. FEMS Microbiology Reviews, 37, 462 – 476. Egholm M, Buchardt O, Christensen L et al. ( 1993 ) PNA hybridizes to complementary oligonucleotides obeying the Watson‐Crick hydrogen‐bonding rules. Nature, 365, 566 – 8. Fu Y, Keats KF, Rivkin RB, Lang AS ( 2013 ) Water mass and depth determine the distribution and diversity of Rhodobacterales in an Arctic marine system. FEMS Microbiology Ecology, 84, 564 – 576. Gilbert JA, Steele JA, Caporaso JG et al. ( 2012 ) Defining seasonal marine microbial community dynamics. ISME Journal, 6, 298 – 308. Gilbert JA, Jansson JK, Knight R ( 2014 ) The Earth Microbiome project: successes and aspirations. BMC Biology, 12, 1 – 4. Gower JC ( 1975 ) Generalized procrustes analysis. Psychometrika, 40, 33 – 51. Hanshew AS, Mason CJ, Raffa KF, Currie CR ( 2013 ) Minimization of chloroplast contamination in 16S rRNA gene pyrosequencing of insect herbivore bacterial communities. Journal of Microbiological Methods, 95, 149 – 155. Jackrel SL, Wootton JT ( 2014 ) Local adaptation of stream communities to intraspecific variation in a terrestrial ecosystem subsidy. Ecology, 95, 37 – 43. IndexNoFollow plant microbiome Proteobacteria aquatic environments PNA clamps Earth microbiome project chloroplast Ecology and Evolutionary Biology Science Article 2017 ftumdeepblue https://doi.org/10.1111/1755-0998.12645 2023-07-31T20:45:11Z Plants in terrestrial and aquatic environments contain a diverse microbiome. Yet, the chloroplast and mitochondria organelles of the plant eukaryotic cell originate from free‐living cyanobacteria and Rickettsiales. This represents a challenge for sequencing the plant microbiome with universal primers, as ~99% of 16S rRNA sequences may consist of chloroplast and mitochondrial sequences. Peptide nucleic acid clamps offer a potential solution by blocking amplification of host‐associated sequences. We assessed the efficacy of chloroplast and mitochondria‐blocking clamps against a range of microbial taxa from soil, freshwater and marine environments. While we found that the mitochondrial blocking clamps appear to be a robust method for assessing animal‐associated microbiota, Proteobacterial 16S rRNA binds to the chloroplast‐blocking clamp, resulting in a strong sequencing bias against this group. We attribute this bias to a conserved 14‐bp sequence in the Proteobacteria that matches the 17‐bp chloroplast‐blocking clamp sequence. By scanning the Greengenes database, we provide a reference list of nearly 1500 taxa that contain this 14‐bp sequence, including 48 families such as the Rhodobacteraceae, Phyllobacteriaceae, Rhizobiaceae, Kiloniellaceae and Caulobacteraceae. To determine where these taxa are found in nature, we mapped this taxa reference list against the Earth Microbiome Project database. These taxa are abundant in a variety of environments, particularly aquatic and semiaquatic freshwater and marine habitats. To facilitate informed decisions on effective use of organelle‐blocking clamps, we provide a searchable database of microbial taxa in the Greengenes and Silva databases matching various n‐mer oligonucleotides of each PNA sequence. Peer Reviewed https://deepblue.lib.umich.edu/bitstream/2027.42/138887/1/men12645.pdf https://deepblue.lib.umich.edu/bitstream/2027.42/138887/2/men12645_am.pdf https://deepblue.lib.umich.edu/bitstream/2027.42/138887/3/men12645-sup-0001-SupInfo.pdf Article in Journal/Newspaper Arctic University of Michigan: Deep Blue Molecular Ecology Resources 17 5 931 942 |