Macrofauna regulate heterotrophic bacterial carbon and nitrogen incorporation in low-oxygen sediments

ISME Journal

Volumn 6, Issue 11, 2012, Pages 2140-2151

  Hunter, William R ^a   Veuger, Bart ^b   Witte, Ursula ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

Author keywords

bacteria; C:N coupling; hydrolysable amino acids; macrofauna; oxygen minimum zone; sediment

Indexed keywords

AMINO ACID; CARBON; NITROGEN; OXYGEN; SEA WATER;

AMINO ACID; ANOXIC CONDITIONS; BACTERIUM; BIOGEOCHEMICAL CYCLE; BIOMARKER; BIOMASS; CARBON; CONTINENTAL MARGIN; GLOBAL CHANGE; HETEROTROPHY; MACROBENTHOS; MARINE SEDIMENT; NITROGEN; ORGANIC MATTER; OXYGEN MINIMUM LAYER; PHYTODETRITUS; SEAFLOOR;

ARTICLE; BACTERIUM; BIOMASS; CHEMISTRY; CLIMATE CHANGE; INDIA; METABOLISM; MICROBIOLOGY; SEA; SEDIMENT;

AMINO ACIDS; BACTERIA; BIOMASS; CARBON; CLIMATE CHANGE; GEOLOGIC SEDIMENTS; INDIA; NITROGEN; OCEANS AND SEAS; OXYGEN; SEAWATER;

ANIMALIA; BACTERIA (MICROORGANISMS); METAZOA;

EID: 84867746293     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2012.44     Document Type: Article

References (61)

1. Andersson JH, Woulds C, Schwartz M, Cowie GL, Levin LA, Soetaert K et al. (2008). Short-term fate of phytodetritus in sediments across the Arabian Sea Oxygen Minimum Zone. Biogeosciences 5: 43-53.
2. Arrieta JM, Herndl GL. (2001). Changes in bacterial betagucosidase diversity during a coastal phytoplankton bloom. Limnol Oceanogr 47: 594-599.
3. Berman T, Bechemin C, Maestrini SY. (1999). Release of ammonium and urea from dissolved organic nitrogen in aquatic ecosystems. Aq Micr Ecol 16: 295-302.
4. Billett DSM, Lampitt RS, Rice AL, Mantoura RFC. (1983). Seasonal sedimentation of phytoplankton to the deepsea benthos. Nature 302: 520-522.
5. Boschker HTS, Middelburg JJ. (2002). Stable isotopes and biomarkers in microbial ecology. FEMS Microbiol Ecol 40: 85-95.
6. Brinch-Iversen J, King GM. (1990). Effects of substrate concentration, growth state, and oxygen availability on relationships among bacterial carbon, nitrogen and phospholipid phosphorus content. FEMS Microbiol Lett 74: 345-355.
7. Buhring SI, Lampadariou N, Moodley L, Tselepides A, Witte U. (2006). Benthic microbial and whole-community responses to different amounts of C-13-enriched algae: In situ experiments in the deep Cretan Sea (Eastern Mediterranean). Limnol Oceanogr 51: 157-165.
8. Cook AA, Lambshead PJD, Hawkins LE, Mitchell N, Levin LA. (2000). Nematode abundance at the oxygen minimum zone in the Arabian Sea. Deep Sea Res Pt II 47: 75-85.
9. Cook PLM, Veuger B, Boer S, Middelburg JJ. (2007). Effect of nutrient availability on carbon and nitrogen incorporation and flows through benthic algae and bacteria in near-shore sandy sediment. Aq Micr Ecol 49: 165-180.
10. Cowie GL, Calvert SE, Pedersen TF, Schulz H, Von Rad U. (1999). Organic content and preservational controls in surficial shelf and slope sediments from the Arabian Sea (Pakistan margin). Mar Geol 161: 23-38.
11. Cowie GL, Hedges JI. (1992). Sources and reactivities of amino acids in a coastal marine environment. Limnol Oceanogr 37: 703-724.
12. Dauwe B, Middelburg JJ. (1998). Amino acids and hexosamines as indicators of organic matter degradation state in North Sea sediments. Limnol Oceanogr 43: 782-798.
13. Devol AH. (1978). Bacterial oxygen uptake kinetics as related to biological processes in the oxygen deficient zones of the oceans. Deep Sea Res 25: 137-146.
14. Evrard V, Cook PLM, Veuger B, Huettel M, Middelburg JJ. (2008). Tracing carbon and nitrogen incorporation and pathways in the microbial community of a photic subtidal sand. Aquat Microb Ecol 53: 257-269.
15. 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 Journal 1: 19-27.
16. Gilbert PM, Garside C, Fuhrman JA, Roman MR. (1991). Time-dependent coupling of inorganic and organic nitrogen uptake and regeneration in the plume of the Chesapeake Bay estuary and its regulation by large heterotrophs. Limnol Oceanogr 36: 895-909.
17. Glud RN, Gundersen JK, Jorgensen BB, Revesbech NP, Schulz HD. (1994). Diffusive and total oxygen uptake of deep-sea sediments in the eastern South Atlantic Ocean: In situ and laboratory measurements. Deep Sea Res Pt I 41: 1767-1788.
18. Gooday AJ, Levin LA, Aranda da Silva A, Bett BJ, Cowie GL et al. (2009). Faunal responses to oxygen gradients on the Pakistan Margin: a comparison of foraminiferans, macrofauna and megafauna. Deep Sea Res Pt II 56: 488-502.
19. Gonsalves MJ, Paropkari AL, Fernandes CEG, Loka Bharathi PA, Krishnakumari L, Fernando V et al. (2011). Predominance of anaerobic bacterial community over aerobic community contribute to intensify 'oxygen minimum zone' in the eastern Arabian Sea. Cont Shelf Res 31: 1224-1235.
20. Guillard RRL. (1975). Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds). Culture of Marine Invertebrate Animals. Plenum: New York, USA, pp 26-60.
21. Hall POJ, Brunnegard J, Hulthe G, Martin WR, Stahl H, Tengberg A. (2007). Dissolved organic matter in abyssal sediments: core recovery artifacts. Limnol Oceanogr 52: 19-31.
22. Helly JJ, Levin LA. (2004). Global distribution of naturally occurring marine hypoxia on continental margins. Deep Sea Res Pt I 51: 1159-1168.
23. Hunter WR, Levin LA, Kitazato H, Witte U. (2012). Macrobenthic assemblage structure and organismal stoichiometry control faunal uptake of phytodetritus in OMZ-impacted sediments. Biogeosci 9: 993-1006.
24. Hunter WR, Oguri K, Kitazato H, Ansari ZA, Witte U. (2011). Epi-benthic megafaunal zonation across an oxygen minimum zone at the Indian continental margin. Deep Sea Res Pt I 58: 699-710.
25. Jeffreys RM, Wolff GA, Cowie GL. (2009). Influence of oxygen on heterotrophic reworking of sedimentary lipids at the Pakistan Margin. Deep Sea Res Pt II 56: 358-375.
26. Jensen MM, Lam P, Revsbech NP, Nagel B, Gaye B, Jetten MSM et al. (2011). Intensive nitrogen loss over the Omani Shelf due to anammox coupled with dissimilatory nitrite reduction to ammonium. ISME Journal 5: 1660-1670.
27. Kaiser K, Benner R. (2005). Hydrolysis-induced racemization of amino acids. Limnol Oceanogr Meth 3: 318-325.
28. Komsta L. (2007). Median-based Linear Models 0.11.
29. Middelburg JJ, Barranguet C, Boschker HTS, Herman PMJ, Moens T, Heip CHR. (2000). The fate of intertidal microphytobenthos carbon: An in situ 13C-labeling study. Limnol Oceanogr 45: 1224-1234.
30. Middelburg JJ, Soetaert K, Herman PMJ. (1997). Empirical relationships for use in global diagenetic models. Deep Sea Res Pt I 44: 327-344.
31. Moodley L, Middelburg JJ, Soetaert K, Boschker HTS, Herman PMJ, Heip CHR. (2005). Similar rapid response to phytodetritus deposition in shallow and deep-sea sediments. J Mar Res 63: 457-469.
32. Moodley L, Nigam R, Ingole B, Prakash Babu C, Panchang R, Nanajkar M et al. (2011). Oxygen minimum seafloor ecological (mal) functioning. J Exp Mar Biol Ecol 398: 91-100.
33. Mulholland MR, Lee C, Glibert PM. (2003). Extracellular enzyme activity and uptake of carbon and nitrogen along an estuarine salinity and nutrient gradient. Mar Ecol Prog Ser 258: 3-17.
34. Nausch M, Kerstan E. (2001). The relationship between dissolved carbohydrates and carbohydrate-degrading enzymes in the salinity gradient of the Pomeranian Bight (southern Baltic). Oceanol 45: 437-452.
35. Nomaki H, Heinz P, Nakatsuka T, Shimanaga M, Ohkouchi N, Ogawa NO et al. (2006). Different ingestion pattern of 13C-labeled bacteria and algae by deep-sea benthic foraminifera. Mar Ecol Prog Ser 310: 95-108.
36. Pantoja S, Lee C. (1994). Cell-surface oxidation of amino acids in seawater. Limnol Oceanogr 39: 1718-1726.
37. Pascal P-Y, Dupuy C, Richard P, Rzeznik-Orignac J, Nipuil N. (2008). Bacterivory of a mudflat nematode community under different environmental conditions. Mar Biol 154: 671-682.
38. Pitcher A, Villanueva L, Hopmans EC, Schouten S, Reichart GJ, Damste JSS. (2011). Niche segregation of ammonia-oxidising archaea and anammox bacteria in the Arabian Sea oxygen minimum zone. ISME J 5: 1896-1904.
39. R Development Core Team (2009). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, Austria.
40. Riedel B, Zuschin M, Haselmair A, Stachowitsch M. (2008). Oxygen depletion under glass: Behavioural responses of benthic macrofauna to induced anoxia in the Northern Adriatic. J Exp Mar Biol Ecol 367: 17-27.
41. Risgaard-Petersen N, Langezaal AM, Ingvardsen S, Schmid MC, Jetten MSM, Op den Camp HJM et al. (2006). Evidence for complete denitrification in a benthic foraminifer. Nature 443: 93-96.
42. Sen PK. (1968). Estimates of regression coefficient based on Kendall's tau. J Am Stat Ass 63: 1379-1389.
43. Schwartz MC, Woulds C, Cowie GL. (2009). Sedimentary denitrification rates across the Arabian Sea oxygen minimum zone. Deep Sea Res Pt II 56: 324-332.
44. Smallwood BJ, Wolff GA, Bett BJ, Smith CR, Hoover D, Gage JD et al. (1999). Megafauna can control the quality of organic matter in marine sediments. Naturwiss 86: 320-324.
45. Stolper DA, Revsbech NP, Canfield DE. (2010). Aerobic growth at nanomolar oxygen concentrations. Proc Natl Acad Sci 107: 18755-18760.
46. Stramma L, Schmidtko S, Levin LA, Johnson GC. (2010). Ocean oxygen minima expansions and their biological impacts. Deep Sea Res Pt I 57: 587-595.
47. Thingstad TF. (1987). Utilization of N, P and organic C by heterotrophic bacteria. I. Outline of a chemostat theory with a consistent concept of 'maintenance' metabolism. Mar Ecol Prog Ser 35: 99-109.
48. Thornton B, Zhang Z, Mayes RW, Hogberg MN, Millwood AJ. (2011). Can gas chromatography combustion isotope ratio mass spectrometry be used to quantify organic compound abundance? Rapid Commun Mass Spectrom 25: 2433-2438.
49. Tobias C, Giblin A, McClelland J, Tucker J, Peterson B. (2003). Sediment DIN fluxes and preferential recycling of benthic microalgal nitrogen in a shallow macrotidal estuary. Mar Ecol Prog Ser 257: 25-36.
50. van Nugteren P, Herman PMJ, Moodley L, Middelburg JJ, Vos M, Heip CHR. (2009). Spatial distribution of detrital resources determines the outcome of competition between bacteria and a facultative detritivorous worm. Limnol Oceanogr 54: 1413-1419.
51. Vandewiele S, Cowie G, Soetaert K, Middelburg JJ. (2009). Amino acid biogeochemistry and organic matter degradation state across the Pakistan margin oxygen minimum zone. Deep Sea Res Pt II 56: 318-334.
52. Veuger B, Eyre BD, Maher D, Middelburg JJ. (2007a). Nitrogen incorporation and retention by bacteria, algae, and fauna in a subtropical intertidal sediment: an in situ 15N-labeling study. Limnol Oceanogr 52: 1930-1942.
53. Veuger B, Middelburg JJ. (2007). Incorporation of nitrogen from amino acids and urea by benthic microbes: role of bacteria versus algae and coupled incorporation of carbon. Aquat Microb Ecol 48: 35-46.
54. Veuger B, Middelburg JJ, Boschker HTS, Houtekamer M. (2005). Analysis of 15N incorporation into D-alanine: A new method for tracing nitrogen uptake by bacteria. Limnol Oceanogr: Meth 3: 230-240.
55. Veuger B, Middelburg JJ, Boschker HTS, Houtekamer M. (2007b). Update of 'Analysis of 15N incorporation into D-alanine: A new method for tracing nitrogen uptake by bacteria' (Veuger et al., 2005, Limnol. Oceanogr. Methods 3: 230-240). Limnol Oceanogr Meth 5: 192-194.
56. Veuger B, Van Oevelen D, Boschker HTS, Middelburg JJ. (2006). Fate of peptidoglycan in an intertidal sediment: an in situ 13C-labeling study. Limnol Oceanogr 51: 1572-1580.
57. Ward BB, Devol AH, Rich JJ, Chang BX, Bulow SE, Naik H et al. (2009). Denitrification as the dominant nitrogen loss process in the Arabian Sea. Nature 461: 78-81.
58. Witte U, Wenzhofer F, Sommer S, Boetius A, Heinz P, Aberle N et al. (2003). In situ experimental evidence of the fate of a phytodetritus pulse at the abyssal sea floor. Nature 424: 763-766.
59. Woulds C, Cowie GL, Levin LA, Andersson JH, Middelburg JJ, Vandewiele S et al. (2007). Oxygen as a control on seafloor biological communities and their roles in sedimentary carbon cycling. Limnol Oceanogr 52: 1698-1709.
60. Woulds C, Schwartz MC, Brand T, Cowie GL, Law G, Mowbray SR. (2009). Porewater nutrient concentrations and benthic nutrient fluxes across the Pakistan margin OMZ. Deep Sea Res Pt II 56: 333-346.
61. Wright PA. (1995). Nitrogen excretion: three end products, many physiological roles. J Exp Biol 198: 273-281.