Bioturbation determines the response of benthic ammonia-oxidizing microorganisms to ocean acidification

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 368, Issue 1627, 2013, Pages

  Laverock, B ^a,b,c   Kitidis, V ^a   Tait, K ^a   Gilbert, J A ^d,e   Osborn, A M ^b,f,g   Widdicombe, S ^a  

^a PLYMOUTH MARINE LABORATORY   (United Kingdom)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^d ARGONNE NATIONAL LABORATORY   (United States)

^e UNIVERSITY OF CHICAGO   (United States)

^f UNIVERSITY OF HULL   (United Kingdom)

^g UNIVERSITY OF LINCOLN   (United Kingdom)

Author keywords

Ammonia oxidation; Bioturbation; Marine sediments; Ocean acidification; Upogebia deltaura

Indexed keywords

AMMONIA; BIOGEOCHEMISTRY; BIOTURBATION; BURROW; CARBON DIOXIDE; DISSOLUTION; MARINE SEDIMENT; NITRIFICATION; OXIDATION; PH; SEAWATER;

AMMONIA; SEA WATER;

ANALYSIS OF VARIANCE; ANIMAL; ARCHAEON; BACTERIA; CHEMISTRY; DECAPODA (CRUSTACEA); GROWTH, DEVELOPMENT AND AGING; HEMOLYMPH; METABOLISM; MICROBIOLOGY; MICROFLORA; OXIDATION REDUCTION REACTION; PH; PHYSIOLOGY; POPULATION DYNAMICS; SEA; SEDIMENT; AMMONIA OXIDATION; ARTICLE; BACTERIUM; BIOTURBATION; MARINE SEDIMENTS; OCEAN ACIDIFICATION; UPOGEBIA DELTAURA;

AMMONIA; ANALYSIS OF VARIANCE; ANIMALS; ARCHAEA; BACTERIA; DECAPODA (CRUSTACEA); GEOLOGIC SEDIMENTS; HEMOLYMPH; HYDROGEN-ION CONCENTRATION; MICROBIOTA; OCEANS AND SEAS; OXIDATION-REDUCTION; POPULATION DYNAMICS; SEAWATER;

AMMONIA OXIDATION; BIOTURBATION; MARINE SEDIMENTS; OCEAN ACIDIFICATION; UPOGEBIA DELTAURA;

EID: 84882960675     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2012.0441     Document Type: Article

References (91)

1. Caldeira K, Wickett ME. 2005 Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J. Geophys. Res. 110, C09S04. (doi:10.1029/ 2004JC002671)
2. Meehl G et al. 2007 Global climate projections. In Climate change 2007: The physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (eds S Solomon, D Qin, M Manning, Z Chen, M Marquis, KB Averyt, M Tignor, HL Miller), pp. 747-845. Cambridge, UK: Cambridge University Press.
3. Liu J, Weinbauer MG, Maier C, Dai M, Gattuso J-P. 2010 Effect of ocean acidification on microbial diversity and on microbe-driven biogeochemistry and ecosystem functioning. Aquat. Microb. Ecol. 61, 291-305. (doi:10.3354/ame01446)
4. Joint I, Doney SC, Karl DM. 2011 Will ocean acidification affect marine microbes? ISME J. 5, 1-7. (doi:10.1038/ismej.2010.79)
5. 2-enriched ocean. Oceanography 22, 128-145. (doi:10.5670/ oceanog.2009.103)
6. Huesemann MH, Skillman AD, Crecelius EA. 2002 The inhibition of marine nitrification by ocean disposal of carbon dioxide. Mar. Poll. Bull. 44, 142-148. (doi:10.1016/S0025-326X (01)00194-1)
7. Beman JM, Chow C-E, King AL, Feng Y, Fuhrman JA, Andersson A, Bates NR, Popp BP, Hutchins DA. 2011 Global declines in oceanic nitrification rates as a consequence of ocean acidification. Proc. Natl Acad. Sci. USA 108, 208-213. (doi:10.1073/pnas. 1011053108)
8. Kitidis V, Laverock B, McNeill LC, Beesley A, Cummings D, Tait K, Osborn AM, Widdicombe S. 2011 Impact of ocean acidification on benthic and water column ammonia oxidation. Geophys. Res. Lett. 38, L21603. (doi:10.1029/2011GL049095)
9. 2 induced acidification in the North Sea. J. Mar. Sys. 64, 229-241. (doi:10.1016/j.jmarsys.2006.03.016)
10. Suzuki I, Abee T, Kwok SC. 1974 Ammonia or ammonium ion as substrate for oxidation by Nitrosomonas europaea cells and extracts. J. Bacteriol. 120, 556-558.
11. Frijlink MJ, Abee T, Laanbroek HJ, Boer WD, Konings WN. 1992 The bioenergetics of ammonia and hydroxylamine oxidation in Nitrosomonas europaea at acid and alkaline pH. Arch. Microbiol. 157, 194-199.
12. Laverock B, Gilbert JA, Tait K, Osborn AM, Widdicombe S. 2011 Bioturbation: impact on the marine nitrogen cycle. Biochem. Soc. Trans. 39, 315-320. (doi:10.1042/BST0390315)
13. Herbert RA. 1999 Nitrogen cycling in coastal marine ecosystems. FEMS Microbiol. Rev. 23, 563-590. (doi:10.1111/j.1574-6976.1999.tb00414.x)
14. Canfield DE, Thampdrup B, Kristensen E. 2005 Aquatic geomicrobiology. Advances in marine biology, vol. 48. London, UK: Elsevier Academic Press.
15. Kristensen E. 2000 Organic matter diagenesis at the oxic/anoxic interface in coastal marine sediments, with emphasis on the role of burrowing animals. Hydrobiologia 426, 1-24. (doi:10.1023/ A:1003980226194)
16. 2-induced seawater acidification on the burrowing activity of Nereis virens and sediment nutrient flux. Mar. Ecol. Prog, Ser. 341, 111-122. (doi:10.3354/ meps341111)
17. Wood HL, Spicer JI, Widdicombe S. 2008 Ocean acidification may increase calcification rates, but at a cost. Proc. R. Soc. B 275, 1767-1773. (doi:10.1098/ rspb.2008.0343)
18. 2 induced seawater acidification on infaunal diversity and sediment nutrient fluxes. Mar. Ecol. Prog. Ser. 379, 59-75. (doi:10.3354/meps07894)
19. Kroeker KJ, Micheli F, Gambi MC, Martz TR. 2011 Divergent ecosystem responses within a benthic marine community to ocean acidification. Proc. Natl Acad. Sci. USA 108, 14 515-14 520. (doi:10.1073/ pnas.1107789108)
20. Griffis RB, Suchanek TH. 1991 A model of burrow architecture and trophic modes in thalassinidean shrimp (Decapoda: Thalassinidea). Mar. Ecol. Prog. Ser. 79, 171-183. (doi:10.3354/ meps079171)
21. Dworschak PC. 2000 Global diversity in the Thalassinidea (Decapoda). J. Crust. Biol. 20, 238-245.
22. Leach WE. 1815 A tabular view of the external characters of four classes of animals, which Linné arranged under Insecta: with the distribution of the genera composing three of these classes into 7 orders. Trans. Linn. Soc. Lond. Zool. 11, 306-400.
23. Tunberg B. 1986 Studies on the population ecology of Upogebia deltaura (Leach) (Crustacea, Thalassinidea). Estuar. Coast. Shelf Sci. 22, 753-765. (doi:10.1016/0272-7714(86)90097-1)
24. Christensen B, Vedel A, Kristensen E. 2000 Carbon and nitrogen fluxes in sediment inhabited by suspension-feeding (Nereis diversicolor) and nonsuspension-feeding (N. virens) polychaetes. Mar. Ecol. Prog. Ser. 192, 203-217. (doi:10.3354/ meps192203)
25. Parry D, Kendall M, Pilgrim D, Jones M. 2003 Identification of patch structure within marine benthic landscapes using a remotely operated vehicle. J. Exp. Mar. Biol. Ecol. 285-286, 497-511. (doi:10.1016/S0022-0981(02)00546-4)
26. Laverock B, Smith CJ, Tait K, Osborn AM, Widdicombe S, Gilbert JA. 2010 Bioturbating shrimp alter the structure and diversity of bacterial communities in coastal marine sediments. ISME J. 4, 1531-1544. (doi:10.1038/ismej.2010.86)
27. Howe RL, Rees AP, Widdicombe S. 2004 The impact of two species of bioturbating shrimp (Callianassa subterranea and Upogebia deltaura) on sediment denitrification. J. Mar. Biol. Ass. UK 84, 629-632. (doi:10.1017/S002531540400966Xh)
28. 2 on the physiology and behaviour of an important ecosystem engineer, the burrowing shrimp Upogebia deltaura. Aquat. Biol. 15, 73-86. (doi:10.3354/ab00408)
29. Grasshoff K. 1983 Determination of nitrite. In Methods of seawater analysis (eds K Grasshof, M Ehrhardt, K Kremling), pp. 139-142, 2nd edn. Weinheim, Germany: Werlag Chemie.
30. 2 measurements. PICES Spec. Publ. 3, 191.
31. Head R, Medina G, Huskin I, Anadon R, Harris R. 2002 Phytoplankton and mesozooplankton distribution and composition during transects of the Azores Subtropical Front. Deep Sea Res. II 49, 4023-4034. (doi:10.1016/S0967-0645(02)00140-6)
32. 2 system calculations. ORNL/CDIAC-105. Oak Ridge, TN: Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory US Department of Energy.
33. Clarke K, Gorley RN. 2006 PRIMER v6: user manual/ tutorial. Plymouth, UK: PRIMER-E.
34. Anderson M, Gorley R, Clarke K. 2008 PERMANOVA+ for PRIMER: guide to software and statistical methods. Plymouth, UK: PRIMER-E.
35. Aller R. 1984 The importance of relict burrow structures and burrow irrigation in controlling sedimentary solute distributions. Geochim. Cosmochim. Acta 48, 1929-1934. (doi:10.1016/ 0016-7037(84)90375-2)
36. Soetaert K, Hofmann AF, Middelburg JJ, Meysman FJR, Greenwood J. 2007 The effect of biogeochemical processes on pH. Mar. Chem. 105, 30-51. (doi:10.1016/j.marchem.2006.12.012)
37. 3 dissolution at the deep-sea floor. Geochim. Cosmochim. Acta 58, 2799-2809. (doi:10.1016/0016-7037(94) 90115-5)
38. 3 dissolution in California continental margin sediments: the influence of organic matter remineralization. Geochim. Cosmochim. Acta 61, 3587-3604. (doi:10.1016/S0016-7037(97)00184-1)
39. 2. Geochim. Cosmochim. Acta 65, 2677-2690. (doi:10.1016/S0016-7037(01)00620-2)
40. Jahnke R, Jahnke DB. 2004 Calcium carbonate dissolution in deep sea sediments: reconciling microelectrode, pore water and benthic flux chamber results. Geochim. Cosmochim. Acta 68, 47-59. (doi:10.1016/S0016-7037(03)00260-6)
41. 2-carbonic acid-carbonate sediment system of the Anthropocene. Glob. Biogeochem. Cycles 20, GB1S92. (doi:10.1029/2005GB002506)
42. 2 and ocean acidification: observations from Devil's Hole, Bermuda. Aquat. Geochem. 13, 237-264. (doi:10. 1007/s10498-007-9018-8)
43. 2 on animal mediated ecosystem function: the modification of sediment nutrient fluxes by burrowing urchins. Mar. Poll. Bull. (doi:10.1016/j.marpolbul.2012.11.008)
44. 2 during experimental blooms of the coccolithophorid Emiliania huxleyi. Glob. Biogeochem. Cycles 19, GB2023. (doi:10.1029/2004GB002318)
45. Engel A, Thoms U, Riebesell U, Rochelle-Newall E, Zondervan I. 2004 Polysaccharide aggregation as a potential sink of marine dissolved organic carbon. Nature 428, 929-932. (doi:10.1038/ nature02453)
46. Van Duyl F, Kop A, Kok A, Sandee A. 1992 The impact of organic matter and macrozoobenthos on bacterial and oxygen variables in marine sediment boxcosms. Neth. J. Sea Res. 29, 343-355. (doi:10. 1016/0077-7579(92)90074-O)
47. Graf G, Schulz R, Peinart R, Meyer-Reil L-A. 1983 Benthic response to sedimentation events during autumn to spring at a shallow-water station in the Western Kiel Bight. Mar. Biol. 77, 235-246. (doi:10.1007/BF00395812)
48. Krause E, Wichels A, Giménez L, Lunau M, Schilhabel MB, Gerdts G. 2012 Small changes in pH have direct effects on marine bacterial community composition: a microcosm approach. PLoS ONE 7, e47035. (doi:10.1371/journal.pone.0047035)
49. 2 concentration on the dynamics of marine heterotrophic bacterioplankton. Limnol. Oceanogr. 51, 1-11. (doi:10.4319/lo.2006. 51.1.0001)
50. Laverock B, Kitidis V, Tait K, Gilbert JA, Osborn AM, Widdicombe S. 2013 Data from: bioturbation determines the response of benthic ammonia oxidising microorganisms to ocean acidification. Dryad Digital Repository. (doi:10.5061/dryad.b98m6)
51. Ray A, Aller R. 1985 Physical irrigation of relict burrows: implications for sediment chemistry. Mar. Geol. 62, 371-379. (doi:10.1016/0025-3227(85)90125-2)
52. Munksby N, Benthien M, Glud RN. 2002 Flowinduced flushing of relict tube structures in the central Skagerrak (Norway). Mar. Biol. 141, 939-945. (doi:10.1007/s00227-002-0874-x)
53. Astall CM, Taylor AC, Atkinson RJA. 1997 Behavioural and physiological implications of a burrow-dwelling lifestyle for two species of upogebiid mud-shrimp (Crustacea: Thalassinidea). Estuar. Coast. Shelf Sci. 44, 155-168. (doi:10.1006/ ecss.1996.0207)
54. Hansen JI, Henriksen K, Blackburn TH. 1981 Seasonal distribution of nitrifying bacteria and rates of nitrification in coastal marine sediments. Microb. Ecol. 7, 297-304. (doi:10.1007/BF02341424)
55. Joye SB, Hollibaugh JT. 1995 Influence of sulfide inhibition of nitrification on nitrogen regeneration in sediments. Science 270, 623-625. (doi:10.1126/ science.270.5236.623)
56. De Boer W, Kowalchuk GA. 2001 Nitrification in acid soils: micro-organisms and mechanisms. Soil. Biol. Biochem. 33, 853-866. (doi:10.1016/S0038-0717 (00)00247-9)
57. Allison SM, Prosser JI. 1993 Ammonia oxidation at low pH by attached populations of nitrifying bacteria. Soil. Biol. Biochem. 25, 935-941. (doi:10. 1016/0038-0717(93)90096-T)
58. Meyer-Reil L-A. 1994 Microbial life in sedimentary biofilms: the challenge to microbial ecologists. Mar. Ecol. Prog. Ser. 112, 303-311. (doi:10.3354/ meps112303)
59. Solan M, Wigham B. 2005 Biogenic particle reworking and bacterial-invertebrate interactions in marine sediments. In Interactions between macroand microorganisms in marine sediments (eds E Kristensen, RR Haese, JE Kostka), pp. 105-124. Washington, DC: American Geophysical Union.
60. Stal LJ. 2010 Microphytobenthos as a biogeomorphological force in intertidal sediment stabilization. Ecol. Eng. 36, 236-245. (doi:10.1016/ j.ecoleng.2008.12.032)
61. Coelho RV, Cooper RA, Rodrigues SDA. 2000 Burrow morphology and behaviour of the mud shrimp Upogebia omissa (Decapoda: Thalassinidea: Upogebiidae). Mar. Ecol. Prog. Ser. 200, 229-240. (doi:10.3354/meps200229)
62. Kristensen E, Kostka JE. 2005 Macrofaunal burrows and irrigation in marine sediment: microbiological and biogeochemical interactions. In Interactions between macro-and microorganisms in marine sediments (eds E Kristensen, RR Haese, JE Kostka), pp. 125-158. Washington, DC: American Geophysical Union.
63. Steward CC, Nold SC, Ringelberg DB, White DC, Lovell CR. 1996 Microbial biomass and community structures in the burrows of bromophenol producing and non-producing marine worms and surrounding sediments. Mar. Ecol. Prog. Ser. 133, 149-165. (doi:10.3354/meps133149)
64. Papaspyrou S, Gregersen T, Cox RP, Thessalou-Legaki M, Kristensen E. 2005 Sediment properties and bacterial community in burrows of the ghost shrimp Pestarella tyrrhena (Decapoda: Thalassinidea). Aquat. Microb. Ecol. 38, 181-190. (doi:10.3354/ame038181)
65. Kinoshita K, Wada M, Kogure K, Furota T. 2008 Microbial activity and accumulation of organic matter in the burrow of the mud shrimp, Upogebia major (Crustacea: Thalassinidea). Mar. Biol. 153, 277-283. (doi:10.1007/s00227-007-0802-1)
66. Lucas FS, Bertru G, Höfle MG. 2003 Characterization of free-living and attached bacteria in sediments colonized by Hediste diversicolor. Aquat. Microb. Ecol. 32, 165-174. (doi:10.3354/ame032165)
67. Wuchter C et al. 2006 Archaeal nitrification in the ocean. Proc. Natl Acad. Sci. USA 103, 12 317-12 322. (doi:10.1073/pnas.0600756103)
68. Lam P, Jensen MM, Lavik G, McGinnis DF, Müller B, Schubert CJ, Amann R, Thamdrup B, Kuypers MMM. 2007 Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proc. Natl Acad. Sci. USA 104, 7104-7109. (doi:10.1073/pnas. 0611081104)
69. Ward BB, O'Mullan GD. 2002 Worldwide distribution of Nitrosococcus oceani, a marine ammoniaoxidizing g-proteobacterium, detected by PCR and sequencing of 16S rRNA and amoA genes. Appl. Environ. Microbiol. 68, 4153-4157. (doi:10.1128/ AEM.68.8.4153-4157.2002)
70. Sintes E, Bergauer K, De Corte D, Yokokawa T, Herndl GJ. 2013 Archaeal amoA gene diversity points to distinct biogeography of ammoniaoxidizing Crenarchaeota in the ocean. Environ. Microbiol. 15, 1647-1658. (doi:10.1111/j.1462-2920.2012.02801.x)
71. Ward BB. 1987 Kinetic studies on ammonia and methane oxidation by Nitrosococcus oceanus. Arch. Microbiol. 147, 126-133. (doi:10.1007/BF00415273)
72. Röling WFM. 2007 Do microbial numbers count? Quantifying the regulation of biogeochemical fluxes by population size and cellular activity. FEMS Microbiol. Ecol. 62, 202-210. (doi:10.1111/j.1574-6941.2007.00350.x)
73. Prosser JI, Nicol GW. 2008 Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ. Microbiol. 10, 2931-2941. (doi:10.1111/j.1462-2920.2008.01775.x)
74. Francis CA, Beman JM, Kuypers MMM. 2007 New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J. 1, 19-27. (doi:10. 1038/ismej.2007.8)
75. Santoro AE, Casciotti KL, Francis CA. 2010 Activity, abundance and diversity of nitrifying archaea and bacteria in the central California Current. Environ. Microbiol. 12, 1989-2006. (doi:10.1111/j.1462-2920.2010.02205.x)
76. Nicol GW, Leininger S, Schleper C, Prosser JI. 2008 The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ. Microbiol. 10, 2966-2978. (doi:10.1111/j.1462-2920.2008.01701.x)
77. Tait K, Laverock B, Widdicombe S. Submitted. Response of an Arctic sediment nitrogen cycling community to increased pCO2.
78. Jones RD, Morita RY. 1985 Low-temperature growth and whole-cell kinetics of a marine ammonium oxidizer. Mar. Ecol. Prog. Ser. 21, 239-243. (doi:10. 3354/meps021239)
79. Prosser JI. 1986 Theoretical and experimental models of nitrification. Nitrification 20, 63-78.
80. Ward BB. 2000 Nitrification and the marine nitrogen cycle. In Microbial ecology of the oceans (ed. DL Kirchman), pp. 427-454, 2nd edn. New York, NY: Wiley-Liss.
81. 3 concentrations near Km: effects of pH and temperature. Water Res. 28, 2561-2566. (doi:10.1016/0043-1354(94) 90074-4)
82. 2 enhances nitrogen fixation and growth in the marine cyanobacterium Trichodesmium. Glob. Change Biol. 13, 1-6. (doi:10.1111/j.1365-2486. 2006.01314.x)
83. Ridgwell A, Zeebe R. 2005 The role of the global carbonate cycle in the regulation and evolution of the Earth system. Earth Planet. Sci. Lett. 234, 299-315. (doi:10.1016/j.epsl.2005.03.006)
84. Wood HL, Widdicombe S, Spicer JI. 2009 The influence of hypercapnia and the infaunal brittlestar Amphiura filiformis on sediment nutrient flux: will ocean acidification affect nutrient exchange? Biogeosciences 6, 2015-2024. (doi:10.5194/bg-6-2015-2009)
85. Godbold JA, Solan M. 2009 Relative importance of biodiversity and the abiotic environment in mediating an ecosystem process. Mar. Ecol. Prog. Ser. 396, 273-282. (doi:10.3354/ meps08401)
86. Teal LR, Bulling MT, Parker ER, Solan M. 2008 Global patterns of bioturbation intensity and mixed depth of marine soft sediments. Aquat. Biol. 2, 207-218. (doi:10.3354/ab00052)
87. Widdicombe S, Austen MC. 2005 Setting diversity and community structure in subtidal sediments: the importance of biological disturbance. In Interactions between macro-and microorganisms in marine sediments. (eds E Kristensen, RR Haese, JE Kostka), pp. 217-232. Washington, DC: American Geophysical Union.
88. Russell BD, Connell SD, Findlay HS, Tait K, Widdicombe S, Mieszkowska N. 2013 Ocean acidification and rising temperatures may increase biofilm primary productivity but decrease grazer consumption. Phil. Trans. R. Soc. B 368, 20120438. (doi:10.1098/rstb.2012.0438)
89. 2 as a resource among competitors for ecosystem dominance. Phil. Trans. R. Soc. B 368, 20120442. (doi:10.1098/rstb.2012.0442)
90. Tatters AO et al. 2013 Short-and long-term conditioning of a temperate marine diatom community to acidification and warming. Phil. Trans. R. Soc. B 368, 20120437. (doi:10.1098/rstb.2012.0437)
91. Godbold JA, Solan M. 2013 Long-term effects of warming and ocean acidification are modified by seasonal variation in species responses and environmental conditions. Phil. Trans. R. Soc. B 368, 20130186. (doi:10.1098/rstb.2013.0186)