Fossilized giant sulfide-oxidizing bacteria from the Devonian Hollard Mound seep deposit, Morocco.

The giant sulfide-oxidizing bacteria are particularly prone to preservation in the rock record, and their fossils have been identified in ancient phosphorites, cherts, and carbonates. This study reports putative spherical fossils preserved in the Devonian Hollard Mound hydrocarbon-seep deposit. Based on petrographical, mineralogical, and geochemical evidence the putative microfossils are interpreted as sulfide-oxidizing bacteria similar to the present-day genus Thiomargarita, which is also found at modern hydrocarbon seeps. The morphology, distribution, size, and occurrence of the fossilized cells show a large degree of similarity to their modern counterparts. Some of the spherical fossils adhere to worm tubes analogous to the occurrence of modern Thiomargarita on the tubes of seep-dwelling siboglinid worms. Fluorapatite crystals were identified within the fossilized cell walls, suggesting the intercellular storage of phosphorus analogous to modern Thiomargarita cells. The preservation of large sulfide-oxidizing bacteria was probably linked to changing biogeochemical processes at the Hollard Mound seep or, alternatively, may have been favored by the sulfide-oxidizing bacteria performing nitrate-dependent sulfide oxidation-a process known to induce carbonate precipitation. The presence of sulfide-oxidizing bacteria at a Devonian hydrocarbon seep highlights the similarities of past and present chemosynthesis-based ecosystems and provides valuable insight into the antiquity of biogeochemical processes and element cycling at Phanerozoic seeps.

Sulfur isotopes of hydrothermal vent fossils and insights into microbial sulfur cycling within a lower Paleozoic (Ordovician-early Silurian) vent community.

Symbioses between metazoans and microbes involved in sulfur cycling are integral to the ability of animals to thrive within deep-sea hydrothermal vent environments; the development of such interactions is regarded as a key adaptation in enabling animals to successfully colonize vents. Microbes often colonize the surfaces of vent animals and, remarkably, these associations can also be observed intricately preserved by pyrite in the fossil record of vent environments, stretching back to the lower Paleozoic (Ordovician-early Silurian). In non-vent environments, sulfur isotopes are often employed to investigate the metabolic strategies of both modern and fossil organisms, as certain metabolic pathways of microbes, notably sulfate reduction, can produce large sulfur isotope fractionations. However, the sulfur isotopes of vent fossils, both ancient and recently mineralized, have seldom been explored, and it is not known if the pyrite-preserved vent organisms might also preserve potential signatures of their metabolisms. Here, we use high-resolution secondary ion mass spectrometry (SIMS) to investigate the sulfur isotopes of pyrites from recently mineralized and Ordovician-early Silurian tubeworm fossils with associated microbial fossils. Our results demonstrate that pyrites containing microbial fossils consistently have significantly more negative δ34 S values compared with nearby non-fossiliferous pyrites, and thus represent the first indication that the presence of microbial sulfur-cycling communities active at the time of pyrite formation influenced the sulfur isotope signatures of pyrite at hydrothermal vents. The observed depletions in δ34 S are generally small in magnitude and are perhaps best explained by sulfur isotope fractionation through a combination of sulfur-cycling processes carried out by vent microbes. These results highlight the potential for using sulfur isotopes to explore biological functional relationships within fossil vent communities, and to enhance understanding of how microbial and animal life has co-evolved to colonize vents throughout geological time.

Metabolically diverse primordial microbial communities in Earth's oldest seafloor-hydrothermal jasper.

The oldest putative fossils occur as hematite filaments and tubes in jasper-carbonate banded iron formations from the 4280- to 3750-Ma Nuvvuagittuq Supracrustal Belt, Québec. If biological in origin, these filaments might have affinities with modern descendants; however, if abiotic, they could indicate complex prebiotic forms on early Earth. Here, we report images of centimeter-size, autochthonous hematite filaments that are pectinate-branching, parallel-aligned, undulated, and containing Fe2+-oxides. These microstructures are considered microfossils because of their mineral associations and resemblance to younger microfossils, modern Fe-bacteria from hydrothermal environments, and the experimental products of heated Fe-oxidizing bacteria. Additional clusters of irregular hematite ellipsoids could reflect abiotic processes of silicification, producing similar structures and thus yielding an uncertain origin. Millimeter-sized chalcopyrite grains within the jasper-carbonate rocks have 34S- and 33S-enrichments consistent with microbial S-disproportionation and an O2-poor atmosphere. Collectively, the observations suggest a diverse microbial ecosystem on the primordial Earth that may be common on other planetary bodies, including Mars.

A late Paleoproterozoic (1.74 Ga) deep-sea, low-temperature, iron-oxidizing microbial hydrothermal vent community from Arizona, USA.

Modern marine hydrothermal vents occur in a wide variety of tectonic settings and are characterized by seafloor emission of fluids rich in dissolved chemicals and rapid mineral precipitation. Some hydrothermal systems vent only low-temperature Fe-rich fluids, which precipitate deposits dominated by iron oxyhydroxides, in places together with Mn-oxyhydroxides and amorphous silica. While a proportion of this mineralization is abiogenic, most is the result of the metabolic activities of benthic, Fe-oxidizing bacteria (FeOB), principally belonging to the Zetaproteobacteria. These micro-organisms secrete micrometer-scale stalks, sheaths, and tubes with a variety of morphologies, composed largely of ferrihydrite that act as sacrificial structures, preventing encrustation of the cells that produce them. Cultivated marine FeOB generally require neutral pH and microaerobic conditions to grow. Here, we describe the morphology and mineralogy of filamentous microstructures from a late Paleoproterozoic (1.74 Ga) jasper (Fe-oxide-silica) deposit from the Jerome area of the Verde mining district in central Arizona, USA, that resemble the branching tubes formed by some modern marine FeOB. On the basis of this comparison, we interpret the Jerome area filaments as having formed by FeOB on the deep seafloor, at the interface of weakly oxygenated seawater and low-temperature Fe-rich hydrothermal fluids. We compare the Jerome area filaments with other purported examples of Precambrian FeOB and discuss the implications of their presence for existing redox models of Paleoproterozoic oceans during the "Boring Billion."

Evidence of Vent-Adaptation in Sponges Living at the Periphery of Hydrothermal Vent Environments: Ecological and Evolutionary Implications.

The peripheral areas of deep-sea hydrothermal vents are often inhabited by an assemblage of animals distinct to those living close to vent chimneys. For many such taxa, it is considered that peak abundances in the vent periphery relate to the availability of hard substrate as well as the increased concentrations of organic matter generated at vents, compared to background areas. However, the peripheries of vents are less well-studied than the assemblages of vent-endemic taxa, and the mechanisms through which peripheral fauna may benefit from vent environments are generally unknown. Understanding this is crucial for evaluating the sphere of influence of hydrothermal vents and managing the impacts of future human activity within these environments, as well as offering insights into the processes of metazoan adaptation to vents. In this study, we explored the evolutionary histories, microbiomes and nutritional sources of two distantly-related sponge types living at the periphery of active hydrothermal vents in two different geological settings (Cladorhiza from the E2 vent site on the East Scotia Ridge, Southern Ocean, and Spinularia from the Endeavour vent site on the Juan de Fuca Ridge, North-East Pacific) to examine their relationship to nearby venting. Our results uncovered a close sister relationship between the majority of our E2 Cladorhiza specimens and the species Cladorhiza methanophila, known to harbor and obtain nutrition from methanotrophic symbionts at cold seeps. Our microbiome analyses demonstrated that both E2 Cladorhiza and Endeavour Spinularia sp. are associated with putative chemosynthetic Gammaproteobacteria, including Thioglobaceae (present in both sponge types) and Methylomonaceae (present in Spinularia sp.). These bacteria are closely related to chemoautotrophic symbionts of bathymodiolin mussels. Both vent-peripheral sponges demonstrate carbon and nitrogen isotopic signatures consistent with contributions to nutrition from chemosynthesis. This study expands the number of known associations between metazoans and potentially chemosynthetic Gammaproteobacteria, indicating that they can be incredibly widespread and also occur away from the immediate vicinity of chemosynthetic environments in the vent-periphery, where these sponges may be adapted to benefit from dispersed vent fluids.

Microbial-tubeworm associations in a 440 million year old hydrothermal vent community.

Microorganisms are the chief primary producers within present-day deep-sea hydrothermal vent ecosystems, and play a fundamental role in shaping the ecology of these environments. However, very little is known about the microbes that occurred within, and structured, ancient vent communities. The evolutionary history, diversity and the nature of interactions between ancient vent microorganisms and hydrothermal vent animals are largely undetermined. The oldest known hydrothermal vent community that includes metazoans is preserved within the Ordovician to early Silurian Yaman Kasy massive sulfide deposit, Ural Mountains, Russia. This deposit contains two types of tube fossil attributed to annelid worms. A re-examination of these fossils using a range of microscopy, chemical analysis and nano-tomography techniques reveals the preservation of filamentous microorganisms intimately associated with the tubes. The microfossils bear a strong resemblance to modern hydrothermal vent microbial filaments, including those preserved within the mineralized tubes of the extant vent polychaete genus Alvinella The Yaman Kasy fossil filaments represent the oldest animal-microbial associations preserved within an ancient hydrothermal vent environment. They allude to a diverse microbial community, and also demonstrate that remarkable fine-scale microbial preservation can also be observed in ancient vent deposits, suggesting the possible existence of similar exceptionally preserved microfossils in even older vent environments.

Gastropods from the Late Jurassic-Early Cretaceous seep deposits in Spitsbergen, Svalbard.

Eleven gastropod species from seven latest Jurassic-earliest Cretaceous hydrocarbon seep deposits from central Spitsbergen, Svalbard are described and illustrated. Six new species and one new genus are introduced. Sassenfjordia gen. nov. is tentatively classified as a naticoid and is characterized by a naticiform gross teleoconch morphology and a large protoconch ornamented with spiral ribs, similar to those present in the subfamily Sininae. The patellogastropod ?Pectinodonta borealis sp. nov. represents the oldest occurrence of pectinodontid limpets in chemosynthesis-based associations. The colloniid Hikidea svalbardensis sp. nov. is the oldest confirmed occurrence of this genus so far. The eucyclid Eucycloidea bitneri sp. nov. is the second report of an occurrence of this genus at hydrocarbon seeps (both of which come from the Paleo-Barents Sea). Abyssomelania sp. is the third known, and the oldest occurrence of this genus. Hudlestoniella hammeri sp. nov. represents another occurrence of this genus at seeps in the Paleo-Barents Sea; its current higher-rank assignment is reviewed herein. It may belong either to the rissoids, as previously suggested, or to the abyssochrysoids (or zygopleurids). A fossil identified as Cretadmete sp. is here classified in the Purpurinidae, a family of stem neogastropods or tonnoideans. The heterobranch Hyalogyrina knorringfjelletensis sp. nov. is the oldest occurrence of hyalogyrinids in chemosynthesis-based associations. Several oldest occurrences of seep taxa in moderately shallow-water seeps in Spitsbergen suggest that the previously questioned onshore-offshore hypothesis of seep and vent colonization should be carefully re-investigated.

Evidence for early life in Earth's oldest hydrothermal vent precipitates.

Although it is not known when or where life on Earth began, some of the earliest habitable environments may have been submarine-hydrothermal vents. Here we describe putative fossilized microorganisms that are at least 3,770 million and possibly 4,280 million years old in ferruginous sedimentary rocks, interpreted as seafloor-hydrothermal vent-related precipitates, from the Nuvvuagittuq belt in Quebec, Canada. These structures occur as micrometre-scale haematite tubes and filaments with morphologies and mineral assemblages similar to those of filamentous microorganisms from modern hydrothermal vent precipitates and analogous microfossils in younger rocks. The Nuvvuagittuq rocks contain isotopically light carbon in carbonate and carbonaceous material, which occurs as graphitic inclusions in diagenetic carbonate rosettes, apatite blades intergrown among carbonate rosettes and magnetite-haematite granules, and is associated with carbonate in direct contact with the putative microfossils. Collectively, these observations are consistent with an oxidized biomass and provide evidence for biological activity in submarine-hydrothermal environments more than 3,770 million years ago.

Geochemistry, faunal composition and trophic structure in reducing sediments on the southwest South Georgia margin.

Despite a number of studies in areas of focused methane seepage, the extent of transitional sediments of more diffuse methane seepage, and their influence upon biological communities is poorly understood. We investigated an area of reducing sediments with elevated levels of methane on the South Georgia margin around 250 m depth and report data from a series of geochemical and biological analyses. Here, the geochemical signatures were consistent with weak methane seepage and the role of sub-surface methane consumption was clearly very important, preventing gas emissions into bottom waters. As a result, the contribution of methane-derived carbon to the microbial and metazoan food webs was very limited, although sulfur isotopic signatures indicated a wider range of dietary contributions than was apparent from carbon isotope ratios. Macrofaunal assemblages had high dominance and were indicative of reducing sediments, with many taxa common to other similar environments and no seep-endemic fauna, indicating transitional assemblages. Also similar to other cold seep areas, there were samples of authigenic carbonate, but rather than occurring as pavements or sedimentary concretions, these carbonates were restricted to patches on the shells of Axinulus antarcticus (Bivalvia, Thyasiridae), which is suggestive of microbe-metazoan interactions.

New records and a new species of bivalve (Mollusca: Bivalvia) from Miocene hydrocarbon seep deposits, North Island, New Zealand.

Fourteen bivalve taxa belonging to 11 families are present in at least 13 early to middle Miocene hydrocarbon seep deposits in the East Coast Basin, North Island, New Zealand. Among these are at least three new species, one of which, Semeloidea (s. l.) bexhavenensis sp. nov. (Lasaeidae), is described here. New distribution data are recorded for bivalve species in the families Limidae, Propeamussiidae, Malleidae and Solemyidae. Additional morphological details of Gigantidas coseli (Mytilidae) and Pratulum quinarium (Cardiidae) are provided based upon previously unrecorded internal shell features. Palaeoecological analysis indicates that bivalves utilized a broad range of modes of life and niches within the New Zealand Miocene seep environment, and no more than ca. 30% of these bivalve species were likely to have been obligate to seeps.

A chemosynthetic weed: the tubeworm Sclerolinum contortum is a bipolar, cosmopolitan species.

BACKGROUND: Sclerolinum (Annelida: Siboglinidae) is a genus of small, wiry deep-sea tubeworms that depend on an endosymbiosis with chemosynthetic bacteria for their nutrition, notable for their ability to colonise a multitude of reducing environments. Since the early 2000s, a Sclerolinum population has been known to inhabit sediment-hosted hydrothermal vents within the Bransfield Strait, Southern Ocean, and whilst remaining undescribed, it has been suggested to play an important ecological role in this ecosystem. Here, we show that the Southern Ocean Sclerolinum population is not a new species, but more remarkably in fact belongs to the species S. contortum, first described from an Arctic mud volcano located nearly 16,000 km away. RESULTS: Our new data coupled with existing genetic studies extend the range of this species across both polar oceans and the Gulf of Mexico. Our analyses show that the populations of this species are structured on a regional scale, with greater genetic differentiation occurring between rather than within populations. Further details of the external morphology and tube structure of S. contortum are revealed through confocal and SEM imaging, and the ecology of this worm is discussed. CONCLUSIONS: These results shed further insight into the plasticity and adaptability of this siboglinid group to a range of reducing conditions, and into the levels of gene flow that occur between populations of the same species over a global extent.

Brachiopods from Late Jurassic-Early Cretaceous hydrocarbon seep deposits, central Spitsbergen, Svalbard.

Late Jurassic-Early Cretaceous (Late Volgian-latest Ryazanian) rhynchonellate brachiopods are described from eight out of 15 hydrocarbon seep deposits in the Slottsmøya Member of the Agardhfjellet Formation in the Janusfjellet to Knorringfjellet area, central Spitsbergen, Svalbard. The fauna comprises rhynchonellides, terebratulides (terebratuloids and loboidothyridoids) and a terebratellidine. The rhynchonellides include: Pseudomonticlarella varia Smirnova; Ptilorhynchia mclachlani sp. nov.; and Ptilorhynchia obscuricostata Dagys. The terebratulides belong to the terebratuloids: Cyrtothyris? sp.; Cyrtothyris aff. cyrta (Walker); Praelongithyris? aff. borealis Owen; and the loboidothyridoids: Rouillieria cf. michalkowii (Fahrenkohl); Rouillieria aff. ovoides (Sowerby); Rouillieria aff. rasile Smirnova; Uralella? cf. janimaniensis Makridin; Uralella? sp.; Pinaxiothyris campestris? Dagys; Placothyris kegeli? Harper et al.; and Seductorithyris septemtrionalis gen. et sp. nov. The terebratellidine Zittelina? sp. is also present. Age determinations for all but one of the brachiopod-bearing seeps are based on associated ammonites. Five of the seep carbonates have yielded Lingularia similis?, and it is the only brachiopod species recorded from two of the seeps. Other benthic invertebrate taxa occurring in the seeps include bivalves, gastropods, echinoderms, sponges, and serpulid and non-serpulid worm tubes. The brachiopod fauna has a strong Boreal palaeobiogeographic signature. Collectively, the Spitsbergen seep rhynchonellate brachiopods exhibit high species richness and low abundance (<100 specimens from 8 seeps). This contrasts markedly with other Palaeozoic---Mesozoic brachiopod-dominated seep limestones where brachiopods are of low diversity (typically monospecific) with a super-abundance of individuals. The shallow water environmental setting for the Spitsbergen seeps supported a diverse shelf fauna, compared to enigmatic Palaeozoic-Mesozoic brachiopod-dominated seeps.

Bivalves from the latest Jurassic-earliest Cretaceous hydrocarbon seep carbonates from central Spitsbergen, Svalbard.

The bivalve fauna from the latest Jurassic-earliest Cretaceous hydrocarbon seep deposits from central Spitsbergen, Svalbard comprises at least 17 species, four of which belong to chemosymbiotic taxa often found at seeps. These are the solemyid Solemya (Petrasma) cf. woodwardiana; Nucinella svalbardensis sp. nov., which belongs to a group of large Nucinella species known from seeps and deep water environments; the lucinid bivalve, Tehamatea rasmusseni sp. nov., included in a genus widely distributed in other Jurassic-Cretaceous seeps; and Cretaxinus hurumi gen. et sp. nov., which is the oldest known thyasirid and is discussed in relation to other large seep-restricted genera in this family. The remaining species in the fauna belong to 'background' genera known from coeval normal marine sediments, mostly from the Boreal area. These include the nuculid Dacromya chetaensis, two new malletiids (Mesosaccella rogovi sp. nov. and M. toddi sp. nov.), the oxytomiid Oxytoma octavia, at least three Buchia species, at least two pectinids, including Camptonectes (Costicamptonectes) aff. milnelandensis and Camptonectes (Camptochlamys) clatrathus, the limid Pseudolimea arctica, the arcticid Pseudotrapezium aff. groenlandicum, and the pholadomyid Goniomya literata. The large number of 'background' species in the bivalve fauna is probably a reflection of the shallow-water setting of the Svalbard seeps. This might also explain the lack of the seep-restricted modiomorphid bivalve Caspiconcha from the fauna. With solemyids, Nucinella, lucinids and thyasirids, the latest Jurassic-earliest Cretaceous bivalve seep fauna of Svalbard contains typical representatives of the Mesozoic bivalve seep faunas, both long established and young evolutionary colonists.

The impact of global warming and anoxia on marine benthic community dynamics: an example from the Toarcian (Early Jurassic).

The Pliensbachian-Toarcian (Early Jurassic) fossil record is an archive of natural data of benthic community response to global warming and marine long-term hypoxia and anoxia. In the early Toarcian mean temperatures increased by the same order of magnitude as that predicted for the near future; laminated, organic-rich, black shales were deposited in many shallow water epicontinental basins; and a biotic crisis occurred in the marine realm, with the extinction of approximately 5% of families and 26% of genera. High-resolution quantitative abundance data of benthic invertebrates were collected from the Cleveland Basin (North Yorkshire, UK), and analysed with multivariate statistical methods to detect how the fauna responded to environmental changes during the early Toarcian. Twelve biofacies were identified. Their changes through time closely resemble the pattern of faunal degradation and recovery observed in modern habitats affected by anoxia. All four successional stages of community structure recorded in modern studies are recognised in the fossil data (i.e. Stage III: climax; II: transitional; I: pioneer; 0: highly disturbed). Two main faunal turnover events occurred: (i) at the onset of anoxia, with the extinction of most benthic species and the survival of a few adapted to thrive in low-oxygen conditions (Stages I to 0) and (ii) in the recovery, when newly evolved species colonized the re-oxygenated soft sediments and the path of recovery did not retrace of pattern of ecological degradation (Stages I to II). The ordination of samples coupled with sedimentological and palaeotemperature proxy data indicate that the onset of anoxia and the extinction horizon coincide with both a rise in temperature and sea level. Our study of how faunal associations co-vary with long and short term sea level and temperature changes has implications for predicting the long-term effects of "dead zones" in modern oceans.

Bone-boring worms: characterizing the morphology, rate, and method of bioerosion by Osedax mucofloris (Annelida, Siboglinidae).

Osedax worms possess unique "root" tissues that they use to bore into bones on the seafloor, but details of the boring pattern and processes are poorly understood. Here we use X-ray micro-computed tomography to investigate the borings of Osedax mucofloris in bones of the minke whale (Balaenoptera acutorostrata), quantitatively detailing their morphological characteristics for the first time. Comparative thin-sections of the borings reveal how the bone is eroded at the sub-millimeter level. On the basis of these results we hypothesize a model of boring that is dependent on the density and microstructure of the bone. We also present evidence of acidic mucopolysaccharides in the mucus of the root tissue, and hypothesize that this plays an important role in the boring mechanism. We discuss the utility of these new data in evaluating Osedax trace fossils and their relevance for O. mucofloris ecology. Measured rates of bone erosion (6% per year) and evidence of enhanced sulfide release from the borings indicate that Osedax worms are important habitat modifiers in whale-fall communities.

Fossil evidence for serpentinization fluids fueling chemosynthetic assemblages.

Among the deep-sea hydrothermal vent sites discovered in the past 30 years, Lost City on the Mid-Atlantic Ridge (MAR) is remarkable both for its alkaline fluids derived from mantle rock serpentinization and the spectacular seafloor carbonate chimneys precipitated from these fluids. Despite high concentrations of reduced chemicals in the fluids, this unique example of a serpentinite-hosted hydrothermal system currently lacks chemosynthetic assemblages dominated by large animals typical of high-temperature vent sites. Here we report abundant specimens of chemosymbiotic mussels, associated with gastropods and chemosymbiotic clams, in approximately 100 kyr old Lost City-like carbonates from the MAR close to the Rainbow site (36 °N). Our finding shows that serpentinization-related fluids, unaffected by high-temperature hydrothermal circulation, can occur on-axis and are able to sustain high-biomass communities. The widespread occurrence of seafloor ultramafic rocks linked to likely long-range dispersion of vent species therefore offers considerably more ecospace for chemosynthetic fauna in the oceans than previously supposed.

Bones as biofuel: a review of whale bone composition with implications for deep-sea biology and palaeoanthropology.

Whales are unique among vertebrates because of the enormous oil reserves held in their soft tissue and bone. These 'biofuel' stores have been used by humans from prehistoric times to more recent industrial-scale whaling. Deep-sea biologists have now discovered that the oily bones of dead whales on the seabed are also used by specialist and generalist scavenging communities, including many unique organisms recently described as new to science. In the context of both cetacean and deep-sea invertebrate biology, we review scientific knowledge on the oil content of bone from several of the great whale species: Balaenoptera musculus, Balaenoptera physalus, Balaenoptera borealis, Megaptera novaeangliae, Eschrichtius robustus, Physeter macrocephalus and the striped dolphin, Stenella coeruleoalba. We show that data collected by scientists over 50 years ago during the heyday of industrial whaling explain several interesting phenomena with regard to the decay of whale remains. Variations in the lipid content of bones from different parts of a whale correspond closely with recently observed differences in the taphonomy of deep-sea whale carcasses and observed biases in the frequency of whale bones at archaeological sites.