Variation in the nitrogen isotopic composition of amino acids in benthic foraminifera: Implications for their adaptation to oxygen-depleted environments

Limnology and Oceanography

Volumn 60, Issue 6, 2015, Pages 1906-1916

  Nomaki, Hidetaka ^a   Chikaraishi, Yoshito ^a   Tsuchiya, Masashi ^a   Toyofuku, Takashi ^a   Suga, Hisami ^a   Sasaki, Yoko ^a   Uematsu, Katsuyuki ^b   Tame, Akihiro ^b   Ohkouchi, Naohiko ^a  

^a JAPAN AGENCY FOR MARINE EARTH SCIENCE AND TECHNOLOGY   (Japan)

^b MARINE WORKS JAPAN LTD   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; AMINO ACID; BATHYAL ZONE; BENTHIC FORAMINIFERA; DENITRIFICATION; ISOTOPIC COMPOSITION; NITRATE; NITROGEN ISOTOPE; PROTEIN; REDOX CONDITIONS; SAMPLING; SEDIMENT-WATER INTERFACE; SHELL; ULTRASTRUCTURE;

HONSHU; JAPAN; KANTO; SAGAMI BAY;

AMMONIA SP.; FORAMINIFERA; GLOBOBULIMINA AFFINIS; UVIGERINA AKITAENSIS;

EID: 84945236049     PISSN: None     EISSN: 19395590     Source Type: Journal    
DOI: 10.1002/lno.10140     Document Type: Article

References (37)

1. Bernhard, J. M. 2003. Potential symbionts in bathyal foraminifera. Science 299: 861. doi: 10.1126/science.1077314
2. Bernhard, J. M., and S. S. Bowser. 2008. Peroxisome proliferation in foraminifera inhabiting the chemocline: An adaptation to reactive oxygen species exposure? J. Eukaryot. Microbiol. 55: 135-144. doi: 10.1111/j.1550-7408.2008.00318.x
3. Bernhard, J. M., K. R. Buck, M. A. Farmer, and S. S. Bowser. 2000. The Santa Barbara Basin is a symbiosis oasis. Nature 403: 77-80. doi: 10.1038/47476
4. Bernhard, J. M., K. R. Buck, and J. P. Barry. 2001. Monterey Bay cold-seep biota: Assemblages, abundance, and ultrastructure of living foraminifera. Deep-Sea Res. II 48: 2233-2249. doi: 10.1016/S0967-0637(01)00017-6
5. Bernhard, J. M., S. T. Goldstein, and S. S. Bowser. 2010. An ectobiont-bearing foraminiferan, Bolivina pacifica, that inhabits microxic pore waters: Cell-biological and paleocea-nographic insights. Environ. Microbiol. 12: 2107-2119. doi: 10.1111/j.1462-2920.2009.02073.x
6. Bernhard, J. M., K. L. Casciotti, M. R. McIlvin, D. J. Beaudoin, P. T. Visscher, and V. P. Edgcomb. 2012. Potential importance of physiologically diverse benthic foraminifera in sedimentary nitrate storage and respiration. J. Geophys. Res. 117: G03002. doi: 10.1029/2012JG001949
7. Braeckman, U., J. Vanaverbeke, M. Vincx, D. van Oevelen, and K. Soetaert. 2013. Meiofauna metabolism in suboxic sediments: Currently overestimated. PLOS One 8: e59289. doi: 10.1371/journal.pone.0059289
8. Chikaraishi, Y., and others. 2009. Determination of aquatic food-web structure based on compound-specific nitrogen isotopic composition of amino acids. Limnol. Oceanogr.: Methods 7: 740-750. doi: 10.4319/lom.2009.7.740
9. Chikaraishi, Y., Y. Takano, N. O. Ogawa, and N. Ohkouchi. 2010. Instrumental optimization for compound-specific nitrogen isotope analysis of amino acids by gas chroma-tography/combustion/isotope ratio mass spectrometry, p. 367-386. In N. Ohkouchi, I. Tayasu, and K. Koba [eds.], Earth, life, and isotopes. Kyoto Univ. Press.
10. Chikaraishi, Y., S. A. Steffan, N. O. Ogawa, N. F. Ishikawa, Y. Sasaki, M. Tsuchiya, and N. Ohkouchi. 2014. High-resolution food webs based on nitrogen isotopic composition of amino acids. Ecol. Evol. 4: 2423-2449. doi: 10.1002/ece3.1103
11. Doane, T. A., and W. R. Horwath. 2003. Spectrophotometric determination of nitrate with a single reagent. Anal. Lett. 36: 2713-2722. doi: 10.1081/AL-120024647
12. Downs, E. E., B. N. Popp, and M. H. Carolyn. 2014. Nitrogen isotope fractionation and amino acid turnover rates in the Pacific white shrimp Litopenaeus vannamei. Mar. Ecol. Prog. Ser. 516: 239-250. doi: 10.3354/meps11030
13. Glud, R. N., H. Stahl, P. Berg, F. Wenzhoefer, K. Oguri, and H. Kitazato. 2009a. In situ microscale variation in distribution and consumption of O2: A case study from a deep ocean margin sediment (Sagami Bay, Japan). Limnol. Oce-anogr. 54: 1-12. doi: 10.4319/lo.2009.54.1.0001
14. Glud, R. N., and others. 2009b. Nitrogen cycling in a deep ocean margin sediment (Sagami Bay, Japan). Limnol. Oce-anogr. 54: 723-734. doi: 10.4319/lo.2009.54.3.0723
15. Gooday, A. J., J. M. Bernhard, L. A. Levin, and S. B. Suhr. 2000. Foraminifera in the Arabian Sea oxygen minimum zone and other oxygen-deficient settings: Taxonomic composition, diversity, and relation to metazoan faunas. Deep-Sea Res. II 47: 25-54. doi: 10.1016/S0967-0645(99)00099-5
16. Høgslund, S., N. P. Revsbech, T. Cedhagen, L. P. Nielsen, and V. A. Gallardo. 2008. Denitrification, nitrate turnover, and aerobic respiration by benthic foraminiferans in the oxygen minimum zone off Chile. J. Exp. Mar. Biol. Ecol. 359: 85-91. doi: 10.1016/j.jembe.2008.02.015
17. Jeffreys, R. M., E. H. Fisher, A. J. Gooday, K. E. Larkin, D. S. M. Billett, and G. A Wolff. 2015. The trophic and metabolic pathways of foraminifera in the Arabian Sea: Evidence from cellular stable isotopes. Biogeosciences 12: 1781-1797. doi: 10.5194/bg-12-1781-2015
18. Koho, K. A., and E. Pma-Ochoa. 2012. Benthic foraminifera: Inhabitants of low-oxygen environments, p. 251-285. In A. V. Altenbach, J. M. Bernhard, and J. Seckbach [eds.], Anoxia: Evidence for eukaryote survival and paleontologi-cal strategies. Springer.
19. Koho, K. A., E. Pina-Ochoa, E. Geslin, and N. Risgaard-Petersen. 2011. Vertical migration, nitrate uptake and denitrification: Survival mechanisms of foraminifers (Globobulimina turgida) under low oxygen conditions. FEMS Microbiol. Ecol. 75: 273-283. doi: 10.1111/j.1574-6941.2010.01010.x
20. Maeda, T., and others. 2012. Algivore or phototroph? Plako-branchus ocellatus (Gastropoda) continuously acquires klep-toplasts and nutrition from multiple algal species in nature. PLoS ONE 7: e42024. doi: 10.1371/journal.pone.0042024
21. McCarthy, M. D., R. Benner, C. Lee, and M. L. Fogel. 2007. Amino acid nitrogen isotopic fractionation patterns as indicators of heterotrophy in plankton, particulate, and dissolved organic matter. Geochim. Cosmochim. Acta. 71: 4727-4744. doi: 10.1016/j.gca.2007.06.061
22. McClelland, J. W., and J. P. Montoya. 2002. Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology 83: 2173-2180. doi: 10.1890/0012-9658(2002)083[2173:TRATNI]2.0.CO;2
23. Moodley, L., J. J. Middelburg, H. T. S. Boschker, G. C. A. Duineveld, R. Pel, P. M. J. Herman, and C. H. R. Heip. 2002. Bacteria and foraminifera: Key players in a short-term deep-sea benthic response to phytodetritus. Mar. Ecol. Prog. Ser. 236: 23-29. doi: 10.3354/meps236023
24. Nomaki, H., P. Heinz, T. Nakatsuka, M. Shimanaga, and H. Kitazato. 2005. Species-specific ingestion of organic carbon by deep-sea benthic foraminifera and meiobenthos: In situ tracer experiments. Limnol. Oceanogr. 50: 134146. doi: 10.4319/lo.2005.50.1.0134
25. Nomaki, H., N. O. Ogawa, N. Ohkouchi, H. Suga, T. Toyofuku, M. Shimanaga, T. Nakatsuka, and H. Kitazato. 2008. Benthic foraminifera as trophic links between phy-todetritus and benthic metazoans: Carbon and nitrogen isotopic evidence. Mar. Ecol. Prog. Ser. 357: 153-164. doi: 10.3354/meps07309
26. Nomaki, H., N. Ohkouchi, P. Heinz, H. Suga, Y. Chikaraishi, N. O. Ogawa, K. Matsumoto, and H. Kitazato. 2009. Degradation of algal lipids by deep-sea benthic foraminifera: An in situ tracer experiment. Deep-Sea Res 1 56: 14881503. doi: 10.1016/j.dsr.2009.04.013
27. Nomaki, H., N. O. Ogawa, Y. Takano, H. Suga, N. Ohkouchi, and H. Kitazato. 2011. Differing utilization of glucose and algal particulate organic matter by deep-sea benthic organisms of Sagami Bay, Japan. Mar. Ecol. Prog. Ser. 431: 11-24. doi: 10.3354/meps09144
28. Nomaki, H., Y. Chikaraishi, M. Tsuchiya, T. Toyofuku, N. Ohkouchi, K. Uematsu, A. Tame, and H. Kitazato. 2014. Nitrate uptake by foraminifera and use in conjunction with endobionts under anoxic conditions. Limnol. Ocean-ogr. 59: 1879-1888. doi: 10.4319/lo.2014.59.6.1879
29. Ohga, T., and H. Kitazato. 1997. Seasonal changes in bathyal foraminiferal populations in response to the flux of organic matter (Sagami Bay, Japan). Terra Nova 9: 33-37. doi: 10.1046/j.1365-3121.1997.d01-6.x
30. Pina-Ochoa, E., and others. 2010. Widespread occurrence of nitrate storage and denitrification among foraminifera and Gromiida. Proc. Natl Acad. Sci. USA 107: 1148-1153. doi: 10.1073/pnas.0908440107
31. Popp, B. N., B. S. Graham, R. J. Olson, C. C. S. Hannides, M. J. Lott, G. A. Lopez-Ibarra, F. Galvan-Magana, and B. Fry. 2007. Insight into the trophic ecology of yellowfin tuna, Thunnus albacares, from compound-specific nitrogen isotope analysis of proteinaceous amino acids, p. 173-190. In T. E. Dawson and R. T. W. Siegwolf [eds.], Stable isotopes as indicators of ecological change. Academic Press.
32. Risgaard-Petersen, N.. 2006. Evidence for complete denitrification in a benthic foraminifer. Nature 443: 93-96. doi: 10.1038/nature05070
33. Shaffer, G., S. M. Olsen, and J. O. P. Pedersen. 2009. Long-term ocean oxygen depletion in response to carbon dioxide emissions from fossil fuels. Nat. Geosci. 2: 105-109. doi: 10.1038/NGEO420
34. Steffan, S. A., Y. Chikaraishi, D. R. Horton, N. Ohkouchi, M. E. Singleton, E. Miliczky, D. B. Hogg, and V. P. Jones. 2013. Trophic hierarchies illuminated via amino acid iso-topic analysis. PLOS One. 8: e76152. doi: 10.1371/journal.pone.0076152
35. Stramma, L., S. Schmidtko, L. Levin, and G. C. Johnson. 2010. Ocean oxygen minima expansions and their biological impacts. Deep-Sea Res. 1 57: 587-595. doi: 10.1016/j.dsr.2010.01.005
36. Toyofuku, T., H. Kitazato, H. Kawahata, M. Tsuchiya, and M. Nohara. 2000. Evaluation of Mg/Ca thermometry in fora-minifera: Comparison of experimental results and measurement in nature. Paleoceanography 15: 456-464. doi: 10.1029/1999PA000460
37. Woulds, C.. 2007. Oxygen as a control on sea-floor biological communities and their roles in sedimentary carbon cycling. Limnol. Oceanogr. 52: 1698-1709. doi: 10.4319/lo.2007.52.4.1698