Abstract Deep-sea methane seeps are dynamic sources of greenhouse gas production and unique habitats supporting ocean biodiversity and productivity. Here, we demonstrate new animal-bacterial symbioses fueled by methane, between two undescribed species of annelid (a serpulid Laminatubus and sabellid Bispira ) and distinct methane-oxidizing Methylococcales bacteria. Worm tissue δ 13 C of −44‰ to −58‰ suggested methane-fueled nutrition for both species and shipboard experiments revealed active assimilation of 13 C-labelled CH 4 into animal biomass, occurring via engulfment of methanotrophic bacteria across the host epidermal surface. These worms represent a new addition to the few animals known to intimately associate with methane-oxidizing bacteria, and further explain their enigmatic mass occurrence at 150-million-year-old fossil seeps. High-resolution seafloor surveys document significant coverage by these symbioses, beyond typical obligate seep fauna. These findings uncover novel consumers of methane in the deep-sea, and by expanding the known spatial extent of methane seeps, may have important implications for deep-sea conservation.
Human-modified habitats are expanding rapidly; many tropical countries have highly fragmented and degraded forests. Preserving biodiversity in these areas involves protecting species-like frugivorous bats-that are important to forest regeneration. Fruit bats provide critical ecosystem services including seed dispersal, but studies of how their diets are affected by habitat change have often been rather localized. This study used stable isotope analyses (δ15N and δ13C measurement) to examine how two fruit bat species in Madagascar, Pteropus rufus (n = 138) and Eidolon dupreanum (n = 52) are impacted by habitat change across a large spatial scale. Limited data for Rousettus madagascariensis are also presented. Our results indicated that the three species had broadly overlapping diets. Differences in diet were nonetheless detectable between P. rufus and E. dupreanum, and these diets shifted when they co-occurred, suggesting resource partitioning across habitats and vertical strata within the canopy to avoid competition. Changes in diet were correlated with a decrease in forest cover, though at a larger spatial scale in P. rufus than in E. dupreanum. These results suggest fruit bat species exhibit differing responses to habitat change, highlight the threats fruit bats face from habitat change, and clarify the spatial scales at which conservation efforts could be implemented.
ABSTRACT Riftia pachyptila is the most conspicuous organism living at deep sea hydrothermal vents along the East Pacific Rise. To support its large size and high growth rates, this invertebrate relies exclusively upon internal chemosynthetic bacterial symbionts. The animal must supply inorganic carbon at high rates to the bacteria, which are far removed from the external medium. We found substantial differences in body fluid total inorganic carbon (ΣCO2) both within and between vent sites when comparing freshly captured worms from a variety of places. However, the primary influence on body fluid ΣCO2 was the chemical characteristics of the site from which the worms were collected. Studies on tubeworms, both freshly captured and maintained in captivity, demonstrate that the acquisition of inorganic carbon is apparently limited by the availability of CO2, as opposed to bicarbonate, and thus appears to be accomplished via diffusion of CO2 into the plume, rather than by mediated transport of bicarbonate. The greatly elevated measured at the vent sites (up to 12.6 kPa around the tubeworms), which is a result of low environmental pH (as low as 5.6 around the tubeworms), and elevated ΣCO2 (as high as 7.1 mmol l−1 around the tubes) speeds this diffusion. Moreover, despite large and variable amounts of internal ΣCO2, these worms maintain their extracellular fluid pH stable, and alkaline, in comparison with the environment. The maintenance of this alkaline pH acts to concentrate inorganic carbon into extracellular fluids. Exposure to N-ethylmaleimide, a non-specific H+-ATPase inhibitor, appeared to stop this process, resulting in a decline in extracellular pH and ΣCO2. We hypothesize that the worms maintain their extracellular pH by active proton-equivalent ion transport via high concentrations of H+-ATPases. Thus, Riftia pachyptila is able to support its symbionts’ large demand for inorganic carbon owing to the elevated in the vent environment and because of its ability to control its extracellular pH in the presence of large inward CO2 fluxes.
The highest oceanic temperatures are found at hydrothermal vents, where the polychaete Paralvinella sulfincola lives on vent sulfides within steep and dynamic thermal gradients. To determine P. sulfincola thermotolerance and preference, we developed a high-pressure aquarium that mimics in situ thermal gradients and permits P. sulfincola to move within the gradient. These polychaetes were thermotaxic, preferring temperatures of 40 degrees to 50 degrees C. Some individuals remained at 50 degrees C for 7 hours (the duration of the experiment), whereas others endured exposure to 55 degrees C for over 15 minutes, demonstrating that alvinellids prefer high temperatures and are among the most thermotolerant of marine organisms.
In many seagrass sediments, lucinid bivalves and their sulfur-oxidizing symbionts are thought to underpin key ecosystem functions, but little is known about their role in nutrient cycles, particularly nitrogen. We used natural stable isotopes, elemental analyses, and stable isotope probing to study the ecological stoichiometry of a lucinid symbiosis in spring and fall. Chemoautotrophy appeared to dominate in fall, when chemoautotrophic carbon fixation rates were up to one order of magnitude higher as compared with the spring, suggesting a flexible nutritional mutualism. In fall, an isotope pool dilution experiment revealed carbon limitation of the symbiosis and ammonium excretion rates up to tenfold higher compared with fluxes reported for nonsymbiotic marine bivalves. These results provide evidence that lucinid bivalves can contribute substantial amounts of ammonium to the ecosystem. Given the preference of seagrasses for this nitrogen source, lucinid bivalves' contribution may boost productivity of these important blue carbon ecosystems.
Continental margins host methane seeps, animal falls and wood falls, with chemosynthetic communities that may share or exchange species. The goal of this study was to examine the existence and nature of linkages among chemosynthesis-based ecosystems by deploying organic fall mimics (bone and wood) alongside defaunated carbonate rocks within high and lesser levels of seepage activity for 7.4 years. We compared community composition, density, and trophic structure of invertebrates on these hard substrates at active methane seepage and transition (less seepage) sites at Mound 12 at ~1,000 m depth, a methane seep off the Pacific coast of Costa Rica. At transition sites, the community composition on wood and bone was characteristic of natural wood- and whale-fall community composition, which rely on decay of the organic substrates. However, at active sites, seepage activity modified the relationship between fauna and substrate, seepage activity had a stronger effect in defining and homogenizing these communities and they depend less on organic decay. In contrast to community structure, macrofaunal trophic niche overlap between substrates, based on standard ellipse areas, was greater at transition sites than at active sites, except between rock and wood. Our observations suggest that whale- and wood-fall substrates can function as stepping stones for seep fauna even at later successional stages, providing hard substrate for attachment and chemosynthetic food.
ABSTRACT The hydrothermal vent tubeworm Riftia pachyptila lacks a mouth and gut and lives in association with intracellular, sulfide-oxidizing chemoautotrophic bacteria. Growth of this tubeworm requires an exogenous source of nitrogen for biosynthesis, and, as determined in previous studies, environmental ammonia and free amino acids appear to be unlikely sources of nitrogen. Nitrate, however, is present in situ (K. Johnson, J. Childress, R. Hessler, C. Sakamoto-Arnold, and C. Beehler, Deep-Sea Res. 35:1723–1744, 1988), is taken up by the host, and can be chemically reduced by the symbionts (U. Hentschel and H. Felbeck, Nature 366:338–340, 1993). Here we report that at an in situ concentration of 40 μM, nitrate is acquired by R. pachyptila at a rate of 3.54 μmol g −1 h −1 , while elimination of nitrite and elimination of ammonia occur at much lower rates (0.017 and 0.21 μmol g −1 h −1 , respectively). We also observed reduction of nitrite (and accordingly nitrate) to ammonia in the trophosome tissue. When R. pachyptila tubeworms are exposed to constant in situ conditions for 60 h, there is a difference between the amount of nitrogen acquired via nitrate uptake and the amount of nitrogen lost via nitrite and ammonia elimination, which indicates that there is a nitrogen “sink.” Our results demonstrate that storage of nitrate does not account for the observed stoichiometric differences in the amounts of nitrogen. Nitrate uptake was not correlated with sulfide or inorganic carbon flux, suggesting that nitrate is probably not an important oxidant in metabolism of the symbionts. Accordingly, we describe a nitrogen flux model for this association, in which the product of symbiont nitrate reduction, ammonia, is the primary source of nitrogen for the host and the symbionts and fulfills the association's nitrogen needs via incorporation of ammonia into amino acids.
Transcriptome profiling by RNA sequencing (RNA-seq) has been widely used to characterize cellular status, but it relies on second-strand complementary DNA (cDNA) synthesis to generate initial material for library preparation. Here we use bacterial transposase Tn5, which has been increasingly used in various high-throughput DNA analyses, to construct RNA-seq libraries without second-strand synthesis. We show that Tn5 transposome can randomly bind RNA/DNA heteroduplexes and add sequencing adapters onto RNA directly after reverse transcription. This method, Sequencing HEteRo RNA-DNA-hYbrid (SHERRY), is versatile and scalable. SHERRY accepts a wide range of starting materials, from bulk RNA to single cells. SHERRY offers a greatly simplified protocol and produces results with higher reproducibility and GC uniformity compared with prevailing RNA-seq methods.
Long‐term observations of faunal communities are essential to identify biological and ecological key phenomena. Observational studies of deep sea habitats such as hydrothermal vents, however, have been restricted by technological limitations. Here we describe our recently developed instrument SMOKE (Submersible Macrophotography Observation Kamera Equipment) that was used for time‐lapse macrophotography synchronized with temperature readings for up to 28 h at 2200 m depth. Lighting was provided by a novel low‐cost white LED array powered by AA or AAA batteries embedded in epoxy within an aluminum case. SMOKE was successfully deployed at the Juan de Fuca ridge in the Northeast Pacific and delivered fine‐resolution pictures as well as centimeter‐scale temperature readings in diffuse vent flow habitats of small motile invertebrates. We found high spatial temperature changes within faunal assemblages and could identify and track specimens down to a size of 2 mm. SMOKE is also characterized by low fabrication and maintenance costs and a straight‐forward, reliable design. Overall, this device proved to be a valuable tool for macrofaunal observations linked with temperature changes over extended time periods.
Loffredo JR, Moore BC, Lee RW, Katz SL, Cross BK. 2019. Trophic status of a non-native crayfish in an oligotrophic lake: Bottom-up view of a mixed warmwater and coldwater sport fishery food web. Lake Reserv Manage. 35:396–414.Numerous studies in recent decades have observed variable trophic status for freshwater crayfish among endemic and exotic populations in lentic or lotic habitats. In this study, we used stable isotope analyses (SIA) to explore trophic status of an introduced population of northern crayfish (Faxonius virilis) in Buffalo Lake, Washington. Northern crayfish are an important prey item for introduced warmwater and coldwater fish species in this lentic system and may buffer competitive interactions between largemouth bass (Micropterus salmoides), rainbow trout (Oncorhynchus mykiss), and kokanee (Oncorhynchus nerka). In 2017, the δ13C and δ15N values of liver samples from 208 crayfish informed proportional diet estimates. Crayfish diets were comprised of 8 littoral sources and were examined for cannibalism, temporal, spatial, and ontogenetic trophic shifts. There was no significant spatial or temporal trophic shift detected in this crayfish population. Seasonal δ15N values among all crayfish size classes mirrored seasonal abundance shifts of littoral macroinvertebrates. A multiple-source stable isotope mixing model and relative trophic positions provided evidence for an ontogenetic trophic shift between juvenile and adult crayfish, from a generalist detritivore to a predatory diet dominated by Chironomidae and Ephemeroptera. The trophic status of Buffalo Lake crayfish may affect salmonid management goals if interspecific competition for food between crayfish and sport fish is biologically significant. Our research is an important first step to understanding crayfish trophic status in a lentic food web, and should inform fish stocking regimes and fishery regulations in management efforts to achieve long-term sustainability of this diverse fishery.
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