Publications

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2016
Pasulka, AL, Levin LA, Steele JA, Case DH, Landry MR, Orphan VJ.  2016.  Microbial eukaryotic distributions and diversity patterns in a deep-sea methane seep ecosystem. Environmental Microbiology. 18:3022-3043.   10.1111/1462-2920.13185   AbstractWebsite

Although chemosynthetic ecosystems are known to support diverse assemblages of microorganisms, the ecological and environmental factors that structure microbial eukaryotes (heterotrophic protists and fungi) are poorly characterized. In this study, we examined the geographic, geochemical and ecological factors that influence microbial eukaryotic composition and distribution patterns within Hydrate Ridge, a methane seep ecosystem off the coast of Oregon using a combination of high-throughput 18S rRNA tag sequencing, terminal restriction fragment length polymorphism fingerprinting, and cloning and sequencing of full-length 18S rRNA genes. Microbial eukaryotic composition and diversity varied as a function of substrate (carbonate versus sediment), activity (low activity versus active seep sites), sulfide concentration, and region (North versus South Hydrate Ridge). Sulfide concentration was correlated with changes in microbial eukaryotic composition and richness. This work also revealed the influence of oxygen content in the overlying water column and water depth on microbial eukaryotic composition and diversity, and identified distinct patterns from those previously observed for bacteria, archaea and macrofauna in methane seep ecosystems. Characterizing the structure of microbial eukaryotic communities in response to environmental variability is a key step towards understanding if and how microbial eukaryotes influence seep ecosystem structure and function.

2014
Zapata-Hernandez, G, Sellanes J, Thurber AR, Levin LA, Chazalon F, Linke P.  2014.  New insights on the trophic ecology of bathyal communities from the methane seep area off Concepcion, Chile (similar to 36 degrees S). Marine Ecology-an Evolutionary Perspective. 35:1-21.   10.1111/maec.12051   AbstractWebsite

Studies of the trophic structure in methane-seep habitats provide insight into the ecological function of deep-sea ecosystems. Methane seep biota on the Chilean margin likely represent a novel biogeographic province; however, little is known about the ecology of the seep fauna and particularly their trophic support. The present study, using natural abundance stable isotopes, reveals a complex trophic structure among heterotrophic consumers, with four trophic levels supported by a diversity of food sources at a methane seep area off Concepcion, Chile (similar to 36 degrees S). Although methanotrophy, thiotrophy and phototrophy are all identified as carbon fixation mechanisms fueling the food web within this area, most of the analysed species (87.5%) incorporate carbon derived from photosynthesis and a smaller number (12%) use carbon derived from chemosynthesis. Methane-derived carbon (MDC) incorporation was documented in 22 taxa, including sipunculids, gastropods, polychaetes and echinoderms. In addition, wide trophic niches were detected in suspension-feeding and deposit-feeding taxa, possibly associated with the use of organic matter in different stages of degradation (e.g. from fresh to refractory). Estimates of Bayesian standard ellipses area (SEA(B)) reveal different isotopic niche breadth in the predator fishes, the Patagonian toothfish Dissostichus eleginoides and the combtooth dogfish Centroscyllium nigrum, suggesting generalist versus specialist feeding behaviors, respectively. Top predators in the ecosystem were the Patagonian toothfish D. eleginoides and the dusky cat shark, Bythaelurus canescens. The blue hake Antimora rostrata also provides a trophic link between the benthic and pelagic systems, with a diet based primarily on pelagic-derived carrion. These findings can inform accurate ecosystem models, which are critical for effective management and conservation of methane seep and adjacent deep-sea habitats in the Southeastern Pacific.

Sapir, A, Dillman AR, Connon SA, Grupe BM, Ingels J, Mundo-Ocampo M, Levin LA, Baldwin JG, Orphan VJ, Sternberg PW.  2014.  Microsporidia-nematode associations in methane seeps reveal basal fungal parasitism in the deep sea. Frontiers in Microbiology. 5   10.3389/fmicb.2014.00043   AbstractWebsite

The deep sea is Earth's largest habitat but little is known about the nature of deep-sea parasitism. In contrast to a few characterized cases of bacterial and protistan parasites, the existence and biological significance of deep-sea parasitic fungi is yet to be understood. Here we report the discovery of a fungus-related parasitic microsporidium, Nematocenator marisprofundi n. gen. n. sp. that infects benthic nematodes at methane seeps on the Pacific Ocean floor. This infection is species-specific and has been temporally and spatially stable over 2 years of sampling, indicating an ecologically consistent host-parasite interaction. A high distribution of spores in the reproductive tracts of infected males and females and their absence from host nematodes' intestines suggests a sexual transmission strategy in contrast to the fecal-oral transmission of most microsporidia. N. mansprofundi targets the host's body wall muscles causing cell lysis, and in severe infection even muscle filament degradation. Phylogenetic analyses placed N. marisprofundi in a novel and basal clade not closely related to any described microsporidia clade, suggesting either that microsporidia-nematode parasitism occurred early in microsporidia evolution or that host specialization occurred late in an ancient deep-sea microsporidian lineage. Our findings reveal that methane seeps support complex ecosystems involving interkingdom interactions between bacteria, nematodes, and parasitic fungi and that microsporidia parasitism exists also in the deep-sea biosphere.

2013
Thurber, AR, Levin LA, Rowden AA, Sommer S, Linke P, Kroger K.  2013.  Microbes, macrofauna, and methane: A novel seep community fueled by aerobic methanotrophy. Limnology and Oceanography. 58:1640-1656.   10.4319/lo.2013.58.5.1640   AbstractWebsite

During the discovery and description of seven New Zealand methane seep sites, an infaunal assemblage dominated by ampharetid polychaetes was found in association with high seabed methane emission. This ampharetid-bed assemblage had a mean density of 57,000 +/- 7800 macrofaunal individuals m(-2) and a maximum wet biomass of 274 g m(-2), both being among the greatest recorded from deep-sea methane seeps. We investigated these questions: Does the species assemblage present within these ampharetid beds form a distinct seep community on the New Zealand margin? and What type of chemoautotrophic microbes fuel this heterotrophic community? Unlike the other macro-infaunal assemblages, the ampharetid-bed assemblage composition was homogeneous, independent of location. Based on a mixing model of species-specific mass and isotopic composition, combined with published respiration measurements, we estimated that this community consumes 29-90 mmol C m(-2) d(-1) of methane-fueled biomass; this is > 290 times the carbon fixed by anaerobic methane oxidizers in these ampharetid beds. A fatty acid biomarker approach supported the finding that this community, unlike those previously known, consumes primarily aerobic methanotrophic bacteria. Due to the novel microbial fueling and high methane flux rates, New Zealand's ampharetid beds provide a model system to study the influence of metazoan grazing on microbially mediated biogeochemical cycles, including those that involve greenhouse gas emissions.

2012
Bernardino, AF, Levin LA, Thurber AR, Smith CR.  2012.  Comparative composition, diversity and trophic ecology of sediment macrofauna at vents, seeps and organic falls. Plos One. 7   10.1371/journal.pone.0033515   AbstractWebsite

Sediments associated with hydrothermal venting, methane seepage and large organic falls such as whale, wood and plant detritus create deep-sea networks of soft-sediment habitats fueled, at least in part, by the oxidation of reduced chemicals. Biological studies at deep-sea vents, seeps and organic falls have looked at macrofaunal taxa, but there has yet to be a systematic comparison of the community-level attributes of sediment macrobenthos in various reducing ecosystems. Here we review key similarities and differences in the sediment-dwelling assemblages of each system with the goals of (1) generating a predictive framework for the exploration and study of newly identified reducing habitats, and (2) identifying taxa and communities that overlap across ecosystems. We show that deep-sea seep, vent and organic-fall sediments are highly heterogeneous. They sustain different geochemical and microbial processes that are reflected in a complex mosaic of habitats inhabited by a mixture of specialist (heterotrophic and symbiont-associated) and background fauna. Community-level comparisons reveal that vent, seep and organic-fall macrofauna are very distinct in terms of composition at the family level, although they share many dominant taxa among these highly sulphidic habitats. Stress gradients are good predictors of macrofaunal diversity at some sites, but habitat heterogeneity and facilitation often modify community structure. The biogeochemical differences across ecosystems and within habitats result in wide differences in organic utilization (i.e., food sources) and in the prevalence of chemosynthesis-derived nutrition. In the Pacific, vents, seeps and organic-falls exhibit distinct macrofaunal assemblages at broad-scales contributing to beta diversity. This has important implications for the conservation of reducing ecosystems, which face growing threats from human activities.

2000
Levin, LA, James DW, Martin CM, Rathburn AE, Harris LH, Michener RH.  2000.  Do methane seeps support distinct macrofaunal assemblages? Observations on community structure and nutrition from the northern California slope and shelf Marine Ecology-Progress Series. 208:21-39.   10.3354/meps208021   AbstractWebsite

Although the conspicuous epifauna of reducing environments are known to exhibit strong morphological, physiological, and nutritional adaptations for life in these habitats, it is less clear whether infaunal organisms do so as well. We examined metazoan macrofauna from methane-seep sediments on the northern California slope (500 to 525 m depth) and from seep and non-seep sediments at 3 locations on the shelf (31 to 53 m depth) to determine whether the community structure and nutritional sources of seep infauna were distinct from those in non-seep, margin sediments. Seep macrofauna consisted mainly of normal slope and shelf species found in productive settings. Several macrofaunal taxa, such as Capitella sp., Diastylopsis dawsoni, and Synidotea angulata, exhibited a preference for seeps. Other taxa, such as the amphipods Rhepoxynius abronius and R, daboius, avoided seeps. Species richness of shelf macrofauna, evaluated by rarefaction and diversity indices (H' and J'), generally did not differ in seep and non-seep sediments. Similarly, stable isotopic composition (delta C-13, delta N-15) Of active seep and non-seep macrofauna did not differ at the 3 shelf sites. Stable isotopic analyses of calcareous material confirmed the presence of methane-influenced pore waters at the slope study site. At one slope clam bed, macrofaunal delta C-13 signatures were lower and delta N-15 values were higher than at another clam bed, inactive slope sediments and shelf sites. However, only 1 of 14 macrofaunal taxa (a dorvilleid polychaete) exhibited isotopic evidence of chemosynthetic nutritional sources. At these sites, seep influence on the ecology of continental margin infauna appears spatially limited and relatively subtle. At their current level of activity, the northern California slope and shelf seeps appear to function as ephemeral, small-scale disturbances that are not sufficiently persistent to allow chemosynthesis-based trophic specialization by most infauna. Rather, we suggest that many of the infauna inhabiting these seep sediments are shelf and slope species preadapted to organic-rich, reducing environments.