Major bacterial contribution to the ocean reservoir of detrital organic carbon and nitrogen

Bacterial biomarkers (D-amino acids and muramic acid) were measured in various organic matter size fractions collected in the North Pacific and North Atlantic, and they were used to quantitatively estimate bacterial contributions to particulate and dissolved organic carbon and nitrogen reservoirs. The origins and yields of biomarkers were determined in cultured marine bacteria, and the results indicated that D-amino acids are derived from numerous macromolecules in addition to peptidoglycan and are not solely from peptidoglycan. Bacterial detritus was a major component of particulate organic matter (POM) and is an important source of submicronsize particles and colloids in the ocean. Peptidoglycan was a substantial component of POM but not of dissolved organic matter (DOM). Compositional differences between POM and DOM primarily reflected the selective incorporation of specific bacterial components into these reservoirs. Autotrophic and heterotrophic bacterial sources were not quantified separately, but the presence of D-aspartic acid (D-Asx) and D-serine (D-Ser) suggested that heterotrophic sources were substantial. The average reactivity of bacterial organic matter was comparable to that of the bulk organic carbon pool. Bacteria were important sources of labile, semilabile, and refractory dissolved organic carbon. Bacterial organic matter accounted for ,25% of particulate and dissolved organic carbon and ,50% of particulate and dissolved organic nitrogen. These results demonstrate the importance of bacteria in regulating the ocean carbon and nitrogen cycles. The global cycles of carbon and nitrogen are driven by photosynthetic carbon fixation and heterotrophic metabolism. Diverse populations of Bacteria, Archaea, and Eukarya control these processes, which are also the main sources of nonliving organic matter in the ocean. The pool of nonliving organic matter in the ocean is one of the largest and most dynamic reservoirs of organic carbon on Earth, yet the relative contributions from Bacteria, Archaea, and Eukarya are unknown. Furthermore, it is unclear whether autotrophic or heterotrophic organisms are dominant contributors to marine organic matter. Eukaryotic plankton dominate autotrophic production in many regions of the oceans, and bacteria play a major role in the autotrophic production in the vast subtropical gyres. Heterotrophic bacteria utilize and transform a large fraction of autotrophic production and thereby contribute to the reservoir of nonliving organic matter in the ocean. Recent reports have presented molecular evidence in support of a major bacterial contribution to nonliving organic matter in the oceans (Tanoue et al. 1995; McCarthy et al. 1998; Benner and Kaiser 2003). Most of the characterized biochemicals specifically occur in the bacterial cell wall–membrane complex. Peptidoglycan is a unique bacterial cell wall heteropolymer, and several studies have indicated that this biopolymer is a ubiquitous constituent of organic matter from freshwater, estuarine, and openocean environments (McCarthy et al. 1998; Dittmar et al. 2001; Jones et al. 2005) and sedimentary organic matter (Lomstein et al. 2006 and references therein). Biomarkers provide a powerful tool for tracing biogenic sources and diagenetic alterations of organic matter. However, the effective use of biomarkers requires intimate knowledge of the abundance and molecular distribution of biomarkers among source organisms and the sensitivity of biomarkers to diagenetic alterations (Hedges and Prahl 1993). Bacteria synthesize a variety of unique organic compounds that can be used as indicators of bacterial contributions to particulate organic matter (POM) and dissolved organic matter (DOM) in the oceans. Many bacterial biomarkers, including D-amino acids and muramic acid (Mur), are commonly found in the cell wall complex of bacteria. Although there is considerable literature available about the occurrence of D-amino acids and Mur in pathogenic bacteria, not much is known about the abundance and distribution of these biomarkers in marine bacteria. A comprehensive survey is needed before D-amino acids and Mur can be applied to estimate bacterial contributions in marine environments. The most useful biomarkers for quantitative determination of bacterial detritus are of similar reactivity as bulk bacterial carbon (C) and nitrogen (N). Few studies provide information on the reactivity of biomarkers relative to bacterial C and N, but existing studies indicate that Damino acids are fairly representative of total bacterial amino acids and bulk C and N (Kawasaki and Benner 2006; Middelboe and Jørgensen 2006). Other laboratory experiments with a mixture of algal and bacterial DOM have shown that D-amino acids and bacterial DOM are less bioreactive than algal DOM (Jørgensen et al. 1999; Amon 1 Corresponding author ([email protected]). Acknowledgments We gratefully acknowledge Nobuyuki Kawasaki for providing field samples and data from the HOT cruise in 2005. We thank Hila Elifantz and Dave Kirchman for providing bacterial cultures, Jenny Davis for insightful discussions, and the crew aboard the Kai-ma-kai O’Kanaloa and Cape Hatteras for assistance with sampling. We thank two anonymous reviewers for helpful comments on an earlier draft of this manuscript. This work was supported by National Science Foundation grant OCE-0080782. Limnol. Oceanogr., 53(1), 2008, 99–112 E 2008, by the American Society of Limnology and Oceanography, Inc.