title: Bioturbation determines the response of benthic ammonia-oxidizing microorganisms to ocean acidification.
abstract: Ocean acidification (OA), caused by the dissolution of increasing concentrations of atmospheric carbon dioxide (CO2) in seawater, is projected to cause significant changes to marine ecology and biogeochemistry. Potential impacts on the microbially driven cycling of nitrogen are of particular concern. Specifically, under seawater pH levels approximating future OA scenarios, rates of ammonia oxidation (the rate-limiting first step of the nitrification pathway) have been shown to dramatically decrease in seawater, but not in underlying sediments. However, no prior study has considered the interactive effects of microbial ammonia oxidation and macrofaunal bioturbation activity, which can enhance nitrogen transformation rates. Using experimental mesocosms, we investigated the responses to OA of ammonia oxidizing microorganisms inhabiting surface sediments and sediments within burrow walls of the mud shrimp Upogebia deltaura. Seawater was acidified to one of four target pH values (pHT 7.90, 7.70, 7.35 and 6.80) in comparison with a control (pHT 8.10). At pHT 8.10, ammonia oxidation rates in burrow wall sediments were, on average, fivefold greater than in surface sediments. However, at all acidified pH values (pH ≤ 7.90), ammonia oxidation rates in burrow sediments were significantly inhibited (by 79-97%; p < 0.01), whereas rates in surface sediments were unaffected. Both bacterial and archaeal abundances increased significantly as pHT declined; by contrast, relative abundances of bacterial and archaeal ammonia oxidation (amoA) genes did not vary. This research suggests that OA could cause substantial reductions in total benthic ammonia oxidation rates in coastal bioturbated sediments, leading to corresponding changes in coupled nitrogen cycling between the benthic and pelagic realms.
authors: Plymouth Marine Laboratory, Prospect Place, Plymouth PL1 3DH, UK. bonnie.laverock@uwa.edu.au
authors: B
authors: B
authors: Laverock
authors: V
authors: V
authors: Kitidis
authors: K
authors: K
authors: Tait
authors: J A
authors: JA
authors: Gilbert
authors: A M
authors: AM
authors: Osborn
authors: S
authors: S
authors: Widdicombe
mesh_terms: D000641:Ammonia / Q000378:metabolism*; D000704:Analysis of Variance; D000818:Animals; D001105:Archaea / Q000254:growth & development / Q000378:metabolism*; D001419:Bacteria / Q000254:growth & development / Q000378:metabolism*; D033364:Decapoda / Q000737:chemistry; D019015:Geologic Sediments / Q000382:microbiology*; D006458:Hemolymph / Q000737:chemistry; D006863:Hydrogen-Ion Concentration; D064307:Microbiota / Q000502:physiology*; D009792:Oceans and Seas; D010084:Oxidation-Reduction; D011157:Population Dynamics; D012623:Seawater / Q000737:chemistry*
chemical_list: D000641:Ammonia
keywords: Upogebia deltaura; ammonia oxidation; bioturbation; marine sediments; ocean acidification
references: Biochem Soc Trans. 2011 Jan;39(1):315-20
references: 21265795
references: Proc Biol Sci. 2008 Aug 7;275(1644):1767-73
references: 18460426
references: Philos Trans R Soc Lond B Biol Sci. 2013 Aug 26;368(1627):20120438
references: 23980241
references: Environ Microbiol. 2008 Nov;10(11):2931-41
references: 18973620
references: ISME J. 2011 Jan;5(1):1-7
references: 20535222
references: Environ Microbiol. 2008 Nov;10(11):2966-78
references: 18707610
references: FEMS Microbiol Ecol. 2007 Nov;62(2):202-10
references: 17614962
references: Proc Natl Acad Sci U S A. 2007 Apr 24;104(17):7104-9
references: 17420469
references: PLoS One. 2012;7(10):e47035
references: 23071704
references: Philos Trans R Soc Lond B Biol Sci. 2013 Aug 26;368(1627):20120441
references: 23980243
references: ISME J. 2007 May;1(1):19-27
references: 18043610
references: Nature. 2004 Apr 29;428(6986):929-32
references: 15118723
references: Philos Trans R Soc Lond B Biol Sci. 2013 Aug 26;368(1627):20130186
references: 23980249
references: Environ Microbiol. 2013 May;15(5):1647-58
references: 22690844
references: Appl Environ Microbiol. 2002 Aug;68(8):4153-7
references: 12147525
references: Philos Trans R Soc Lond B Biol Sci. 2013 Aug 26;368(1627):20120437
references: 23980240
references: Philos Trans R Soc Lond B Biol Sci. 2013 Aug 26;368(1627):20120442
references: 23980244
references: J Bacteriol. 1974 Oct;120(1):556-8
references: 4422399
references: FEMS Microbiol Rev. 1999 Oct;23(5):563-90
references: 10525167
references: Mar Pollut Bull. 2002 Feb;44(2):142-8
references: 11981978
references: Proc Natl Acad Sci U S A. 2011 Aug 30;108(35):14515-20
references: 21844331
references: Mar Pollut Bull. 2013 Aug 30;73(2):416-27
references: 23218873
references: Microb Ecol. 1981 Dec;7(4):297-304
references: 24227545
references: Proc Natl Acad Sci U S A. 2011 Jan 4;108(1):208-13
references: 21173255
references: ISME J. 2010 Dec;4(12):1531-44
references: 20596074
references: Environ Microbiol. 2010 Jul;12(7):1989-2006
references: 20345944
references: Proc Natl Acad Sci U S A. 2006 Aug 15;103(33):12317-22
references: 16894176