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2012
Thurber, AR, Levin LA, Orphan VJ, Marlow JJ.  2012.  Archaea in metazoan diets: implications for food webs and biogeochemical cycling. ISME Journal. 6:1602-1612.   10.1038/ismej.2012.16   AbstractWebsite

Although the importance of trophic linkages, including 'top-down forcing', on energy flow and ecosystem productivity is recognized, the influence of metazoan grazing on Archaea and the biogeochemical processes that they mediate is unknown. Here, we test if: (1) Archaea provide a food source sufficient to allow metazoan fauna to complete their life cycle; (2) neutral lipid biomarkers (including crocetane) can be used to identify Archaea consumers; and (3) archaeal aggregates are a dietary source for methane seep metazoans. In the laboratory, we demonstrated that a dorvilleid polychaete, Ophryotrocha labronica, can complete its life cycle on two strains of Euryarchaeota with the same growth rate as when fed bacterial and eukaryotic food. Archaea were therefore confirmed as a digestible and nutritious food source sufficient to sustain metazoan populations. Both strains of Euryarchaeota used as food sources had unique lipids that were not incorporated into O. labronica tissues. At methane seeps, sulfate-reducing bacteria that form aggregations and live syntrophically with anaerobic-methane oxidizing Archaea contain isotopically and structurally unique fatty acids (FAs). These biomarkers were incorporated into tissues of an endolithofaunal dorvilleid polychaete species from Costa Rica (mean bulk delta C-13 = -92 +/- 4 parts per thousand; polar lipids -116 parts per thousand) documenting consumption of archaeal-bacterial aggregates. FA composition of additional soft-sediment methane seep species from Oregon and California provided evidence that consumption of archaeal-bacterial aggregates is widespread at methane seeps. This work is the first to show that Archaea are consumed by heterotrophic metazoans, a trophic process we coin as 'archivory'. The ISME Journal (2012) 6, 1602-1612; doi:10.1038/ismej.2012.16; published online 8 March 2012

2005
Levin, LA.  2005.  Ecology of cold seep sediments: Interactions of fauna with flow, chemistry and microbes. Oceanography and Marine Biology - an Annual Review, Vol. 43. 43( Gibson RN, Atkinson RJA, Gordon JDM, Eds.).:1-46., Boca Raton: Crc Press-Taylor & Francis Group Abstract

Cold seeps occur in geologically active and passive continental margins, where pore waters enriched in methane are forced upward through the sediments by pressure gradients. The advective supply of methane leads to dense microbial communities with high metabolic rates. Anaerobic methane oxidation presumably coupled to sulphate reduction facilitates formation of carbonates and, in many places, generates extremely high concentrations of hydrogen sulphide in pore waters. Increased food supply, availability of hard substratum and high concentrations of methane and sulphide supplied to free-living and symbiotic bacteria provide the basis for the complex ecosystems found at these sites. This review examines the structures of animal communities in seep sediments and how they are shaped by hydrologic, geochemical and microbial processes. The full size range of biota is addressed but emphasis is on the mid-size sediment-dwelling infauna (foraminiferans, metazoan meiofauna and macrofauna), which have received less attention than megafauna or microbes. Megafaunal biomass at seeps, which far exceeds that of surrounding non-seep sediments, is dominated by bivalves (mytilids, vesicomyids, lucinids and thyasirids) and vestimentiferan tube worms, with pogonophorans, cladorhizid sponges, gastropods and shrimp sometimes abundant. In contrast, seep sediments at shelf and upper slope depths have infaunal densities that often differ very little from those in ambient sediments. At greater depths, seep infauna exhibit enhanced densities, modified composition and reduced diversity relative to background sediments. Dorvilleid, hesionid and ampharetid polychaetes, nematodes, and calcareous foraminiferans are dominant. There is extensive spatial heterogeneity of microbes and higher organisms at seeps. Specialized infaunal communities are associated with different seep habitats (microbial mats, clam beds, mussel beds and tube worms aggregations) and with different vertical zones in the sediment. Whereas fluid flow and associated porewater properties, in particular sulphide concentration, appear to regulate the distribution, physiological adaptations and sometimes behaviour of many seep biota, sometimes the reverse is true. Animal-microbe interactions at seeps are complex and involve symbioses, heterotrophic nutrition, geochemical feedbacks and habitat structure. Nutrition of seep fauna varies, with thiotrophic and methanotrophic symbiotic bacteria fueling most of the megafaunal forms but macrofauna and most meiofauna are mainly heterotrophic. Macrofaunal food sources are largely photosynthesis-based at shallower seeps but reflect carbon fixation by chemosynthesis and considerable incorporation of methane-derived C at deeper seeps. Export of seep carbon appears to be highly localized based on limited studies in the Gulf of Mexico. Seep ecosystems remain one of the ocean's true frontiers. Seep sediments represent some of the most extreme marine conditions and offer unbounded opportunities for discovery in the realms of animal-microbe-geochemical interactions, physiology, trophic ecology, biogeography, systematics and evolution.

1994
Blair, NE, Plaia GR, Boehme SE, Demaster DJ, Levin LA.  1994.  The remineralization of organic carbon on the North Carolina continental slope. Deep-Sea Research Part Ii-Topical Studies in Oceanography. 41:755-766.   10.1016/0967-0645(94)90046-9   AbstractWebsite

The sources and fates of metabolizable organic carbon were examined at three sites on the North Carolina slope positioned offshore of Cape Fear, Cape Lookout and Cape Hatteras. The C-13/C-12 compositions (delta(13)C) of the solid phase organic matter, and the dissolved inorganic carbon (Sigma CO2) produced during its oxidation, suggested that the labile fraction was predominantly marine in origin. The Sigma CO2 concentration gradient across the sediment-water interface, and by inference the Sigma CO2 flux and production rate, increased northward from Cape Fear to Cape Hatteras. Methane distributions and Sigma CO2 delta(13)C values suggest that the rate of anaerobic diagenesis increased northward as well. The differences in sedimentary biogeochemistry are most likely driven by an along-slope gradient of reactive organic carbon flux to the seabed. This trend in reactive organic carbon flux correlates well with macrofaunal densities previously observed at the three sites. Proximity to the shelf and the transport of particulate material by surface boundary currents may control the deposition of metabolizable material on the Carolina slope. Evidence for methanogenesis was found only on the Cape Hatteras slope. The methane, which was produced at a depth of approximately 1 m in the seabed, was consumed nearly quantitatively in the biologically mixed layer as it diffused upward. Irrigation of the sediments by infauna may have provided the necessary oxidant for the consumption of the methane.