This thesis centres around two genera of large peltospirid gastropods (Mollusca: Neomphalina: Peltospiridae) endemic to hydrothermal vent ecosystems. One is the 'scaly-foot gastropod', an emblematic species of the Indian Ocean vents with unique dermal sclerites covering the foot like roof tiles. The other was recently discovered from expeditions to the Southern and Indian oceans, lacks sclerites and possesses large opercula. As both genera and their assigned species remained undescribed, they were formally described herein which forms a basis to understanding their biology. The 'scaly-foot gastropod' from both the Central Indian Ridge (CIR) and the Southwest Indian Ridge (SWIR) were confirmed to represent a single species and is formally named as Chrysomallon squamiferum. Through molecular genetic analyses using the COI gene, genetic differentiation between SWIR and CIR populations was detected for the 'scaly-foot gastropod'. In contrast, the peltospirids with large opercula from the East Scotia Ridge (ESR) and the SWIR proved to be two distinct species within an undescribed genus. The ESR species was formally described as Gigantopelta chessoia and the SWIR species as G. aegis. The molecular genetic analyses of the COI gene, confirmed the genetic isolation of the two and consolidated their status as separate species. A 3D tomographic model of Chrysomallon squamiferum was generated to characterise the soft anatomy and morphology as well as to understand its internal anatomy and adaptation which remained little-studied. Further to the enlarged esophageal gland already known to house chemosynthetic endosymbionts, C. squamiferum was discovered to have a hypertrophied circulatory system with a gigantic, muscular heart and large ctenidium to adapt to life in a hypoxic environment and to supply the endosymbionts with necessary chemicals. Histological examinations of the sclerites and operculum showed that it was unlikely that the sclerites originated from operculum duplication. Comparisons with polyplacophoran scales revealed starkly different secretion mechanisms despite the superficial similarity, which has implications on the placement of sclerite-bearing Cambrian taxa. Overall, the results from this thesis ascertained the systematic positions of these large-sized, enigmatic peltospirids, and led to improved understanding of their ecology and evolution. The important role of larval dispersal in maintaining metapopulations across the distribution of a vent-endemic taxa is highlighted. The adaptations of vent-endemic taxa remains little-known even in well-studied species, warranting future studies on these and other species.

Thesis: Ph. D., Joint Program in Oceanography/Applied Ocean Science and Engineering (Massachusetts Institute of Technology, Department of Biology; and the Woods Hole Oceanographic Institution), 2016. / Cataloged from PDF version of thesis. / Includes bibliographical references (pages 145-161). / Chemoautotrophic ecosystems at deep-sea hydrothermal vents were discovered in 1977, but not until 1995 were free-living autotrophic Epsilonproteobacteria identified as important microbial community members. Because the deep-sea is food-starved, the autotrophic metabolism of hydrothermal vent Epsilonproteobacteria may be very important for deep-sea consumers. However, quantifying their metabolic activities in situ has remained difficult, and biochemical mechanisms underlying their autotrophic physiology are poorly described. To gain insight into environmental processes, an approach was developed for incubations of microbes at in situ pressure and temperature (25 MPa, 24°C) with various combinations of electron donors/acceptors (H₂ , O₂ and NO₃- and ¹³HCO₃-) as a tracer to track carbon fixation. During short (18-24 h) incubations of low-temperature vent fluids from Crab Spa (9°N East Pacific Rise), the concentration of electron donors/acceptors and cell numbers were monitored to quantify microbial processes. Measured rates were generally higher than previous studies, and the stoichiometry of microbially-catalyzed redox reactions revealed new insights into sulfur and nitrogen cycling. Single-cell, taxonomically-resolved tracer incorporation showed Epsilonproteobacteria dominated carbon fixation, and their growth efficiency was calculated based on electron acceptor consumption. Using these data, in situ primary productivity, microbial standing stock, and average biomass residence time of the deep-sea vent subseafloor biosphere were estimated. Finally, the population structures of the most abundant genera Sulfurimonas and Thioreductor were shown to be strongly influenced by pO₂ and temperature respectively, providing a mechanism for niche differentiation in situ. To gain insights into the core biochemical reactions underlying autotrophy in Epsilonprotebacteria, a theoretical metabolic model of Sulfurimonas denitrificans was developed. Validated iteratively by comparing in silico yields with data from chemostat experiments, the model generated hypotheses explaining critical, yet so far unresolved reactions supporting chemoautotrophy in Epsilonproteo bacteria. For example, it provides insight into how energy is conserved during sulfur oxidation coupled to denitrification, how reverse electron transport produces ferredoxin for carbon fixation, and why aerobic growth yields are only slightly higher compared to denitrification. As a whole, this thesis provides important contributions towards understanding core mechanisms of chemoautrophy, as well as the in situ productivity, physiology and ecology of autotrophic Epsilonproteobacteria. / by Jesse Christopher McNichol. / Ph. D.

Researchers have learned much about the biological assemblages that form around hydrothermal vents. However, identities of species in these assemblages and their basic ecological features are often lacking. In 2015, the first leg of the Hydrothermal Hunt expedition identified likely new vent sites in the Mariana Back-arc Spreading Center (BASC). In 2016, the second leg of the expedition used a remotely operated vehicle (ROV) to confirm and sample two new sites and two previously known sites. My first objective is to identify the animals collected from these four vent sites. In these samples, I identify 42 animal taxa, including the discovery of four new vent-associated species, five potentially new species and six taxa not previously reported in the Mariana BASC vents. My second objective is to combine these new data with previous studies and examine the species distributions among all known vent sites in the Mariana BASC using the α-, β-, and γ-diversity framework. I present updated species absence-presence lists for all eight Mariana BASC vent sites, which begin to resolve some of the issues with species identification. In this thesis, my approach to assessing β-diversity is novel in the field of hydrothermal vent ecology. My work also provides the first intra-regional scale assessments of β-diversity that include all sites known in a vent system. My third objective is to explore environmental factors driving these species distribution patterns. The α-diversity of BASC vent sites gradually increases with latitude, and the β-diversity calculated using the Raup-Crick index correlates with distance to nearby vent sites. Stochastic assembly processes likely shape the diversity patterns throughout the Mariana BASC as few environmental variables are known to correlate with these patterns. My fourth objective is to compare the β-diversity patterns between the Mariana BASC vent sites and those in two other vent systems: the Mariana Arc and the Juan de Fuca Ridge. The γ- and average α-diversity values for the BASC vents are relatively low compared to the other two systems. The Jaccard index revealed that the average number of shared species among the Arc vent sites is much lower than those of the BASC and the Juan de Fuca Ridge. The Raup-Crick index indicates that stochastic processes explain the average β-diversity of the Mariana BASC vents better than those of the Mariana Arc and Juan de Fuca Ridge. / Graduate / 2021-04-17

Here we investigate sedimentological responses to past climate change in shallow to deep marine depositional environments. Our primary study spans from the Late Pliocene to the Pleistocene (3.3 to 0.7 Ma), and features results from two International Ocean Discovery Program (IODP) Sites U1525 and U1524. Each of these sites is discussed in separate chapters here (Chapters 1 and 2). This interval experienced the change from the warming of the Late Pliocene, known as the Mid-Piacenzian Warming Period, to the Pleistocene cooling. This shift significantly impacted the expansion of the West Antarctic Ice Sheet, sea ice/polynya formation, and, notably, the genesis of Antarctic Bottom Water (AABW), a crucial component of the global thermohaline circulation. In Chapter 1, we propose that turbidite currents, arising from the formation of dense shelf water (DSW) in the Ross Sea (a precursor to AABW), leave a distinct record in the levees of Hillary Canyon. This canyon acts as a conduit, channeling DSW into the deep ocean and contributing to AABW production. By analyzing turbidite beds based on their frequency, thickness, and grain size, we gain insights into the historical occurrence and magnitude of these currents. Furthermore, we explore the influence of factors such as shelf availability and sea ice/polynya formation within the broader climate context of AABW formation. Chapter 2 shifts its focus to the sedimentological variability from shelf-to-slope along Hillary Canyon. This chapter examines the turbidite record associated with AABW formation within the shared timeframe (2.1 to 0.7 million years ago) between IODP Sites U1524 and U1525, and the impact of along slope currents and other processes in the sedimentary deposition and transport. The second study interval (Chapter 3), focuses on the regional sedimentological response proximal to a hydrothermal vent complex associated with the Paleocene-Eocene Thermal Maximum (PETM; ca. 56 Ma), a global warming event during which thousands of Gt C was released into the ocean-atmosphere on Kyr timescales. IODP Site U1568, strategically located near the hydrothermal vent complex and part of a broader drilling transect in the Modgunn Arch, North Atlantic, is the main study subject. This site's proximity to the vent complex offers a distinctive environment for refining our understanding of stratigraphy and sedimentology within the PETM. We achieve this through a comprehensive analysis of grain size and composition, coupled with a comparison to XRF data. Our findings show that the timing between the onset of the PETM and the response of the sedimentary system to the warming, reflected in the grain size coarsening after the start of the PETM, is not synchronous. Notably, the transition from a marine to a more terrestrial composition predates this shift in grain size, aligning with the PETM onset instead. / Doctor of Philosophy / Deep-marine core records are invaluable sources of sedimentological information that provide insights into the ocean's response to past climates. These cores, extracted from the deep-ocean floor, contain layers of sediment that accumulate over time because of the different processes that occur in the ocean. Analyzing these sediments, by looking at their physical characteristics like how frequently are they deposited, the thickness of the layers, their grain size, and their composition helps to reconstruct past environmental conditions and understand how the oceans have responded to climatic changes. This dissertation focuses on studying the record of two main processes. The first one is the sedimentary record left behind by the formation of Antarctic Bottom Water (AABW), one of the coldest (-1°C), deepest (> 2000 meters below sea level), and densest water masses in the ocean. AABW is a key component of the global ocean circulation system, often referred to as the "global conveyor belt" or the thermohaline circulation. This circulation pattern plays a crucial role in redistributing heat, salt, and nutrients around the world's oceans. AABW is formed near Antarctica through a process that begins with the cooling and sinking of surface waters near the continent. As these waters sink, they become denser and eventually form AABW, filling the deep ocean basins around Antarctica. The dense water flows from the surface to the bottom of the ocean forming turbidity currents. These turbidity currents, dense plumes of water and sediments, flow down submarine conduits, such as Hillary Canyon in the Ross Sea, Antarctica, leaving a sedimentary record in the levees or flanks, called turbidites. The turbidite sequences in sediment cores can reveal information about the frequency and magnitude of these currents, providing insights into the sediment transport processes in deep-marine settings, and for this work, the history of the AABW formation over the last 3.3 Ma. This study will help to understand what are the main controls for AABW formation across different climates in the past, and how we project this into the future climate scenarios. In the second part of the study (Chapter 3), we look at the sedimentary record of a warming event that happened around 56 million years ago. This event, known as the Paleocene-Eocene Thermal Maximum (PETM), involved a significant amount of carbon being released into the air and oceans over thousands of years (150,000 to 200,000). Our focus is IODP Site U1568, located near a submarine hydrothermal vent, and part of a larger drilling transect in the North Atlantic's Modgunn Arch. The vent's unique location provides a crucial perspective for understanding how the system responded to the warming during the Paleocene-Eocene Thermal Maximum (PETM). This warming event was triggered by the release of carbon into the atmosphere, with the vent serving as one of the conduits for this release. To understand this, we studied the grain size and content of the sediment, and compared that with XRF data. Changes in grain size serve as indicators of shifts in the energy of the environment – coarser grains signify a more energetic system. Warmer weather, for instance, can increase precipitation, leading to more erosion and sediment influx into the basin. This influx also brings in more materials from the land, as evidenced by the presence of microfossils and plant fragments. Our discoveries indicate that the sedimentary system responded gradually to the PETM, as reflected in the coarsening of grain size after the PETM's onset. Notably, the transition from a marine to a more terrestrial composition occurred before the change in grain size, aligning more closely with the initiation of the PETM itself.

This project used a variety of genetic markers to investigate the evolution and population genetics of hydrothermal vent fauna that were recovered from the Scotia Sea, in the Atlantic sector of the Southern Ocean. The origins of one of these species, an undescribed species of Kiwa sp. found on the East Scotia Ridge (ESR) and its constituent family Kiwaidae, a group of vent and seep-associated decapod squat lobsters (infraorder Anomura) was investigated using a concatenated nine-gene dataset and key divergences were dated using fossil calibrations. These results confirm earlier research showing Kiwaidae reside in the superfamily Chirostyloidea, but form a monophyletic clade with the non-chemosynthetic family Chirostylidae and not Eumunididae. Chirostyloid families diverged in the Cretaceous, although extant Kiwaidae radiated in the Eocene, consistent with many other chemosynthetic taxa that appear recently derived. The basal tree position of Pacific species (and the Alaska location of a likely stem-lineage kiwaid fossil) suggests kiwaids originated in the East Pacific. Within a Southern Hemisphere clade, the divergence between the southeastern Pacific K. hirsuta and a non-Pacific lineage (Kiwa sp. ESR and Southwest Indian Ridge kiwaids) is no earlier than 25.9 Ma, consistent with a spread from the Pacific into the Scotia Sea and beyond via now-extinct active ridge connections or mediated by a Miocene onset of the Antarctic Circumpolar Current (ACC) through a newly-opened Drake Passage. This project also investigated the population genetics of three undescribed species found at two vent fields ~ 440 km apart at either end of the ESR: Kiwa sp., a peltospirid gastropod and Lepetodrilus sp. limpets. Lepetodrilus sp. was also found at the Kemp Caldera, a submerged part of the South Sandwich Islands (SSI). Analyses of cytochrome c oxidase subunit 1 (COI) as well as microsatellite loci developed from Roche 454 sequence libraries revealed no differentiation along the ESR for all three species consistent with panmixia, or the dominance of non-equilibrium processes between vent field colonies within a metapopulation, possibly enhanced further by cold-induced arrested larval development. Despite apparent connectivity along the ESR, both COI and microsatellites revealed differentiation between ESR limpets and Kemp Caldera limpets ~ 95 km to the east, possibly owing to the hydrographic isolation of the caldera. Both COI and microsatellite diversity patterns were consistent with recent (< 1 Ma) demographic expansions for all three species (although the influence of selection sweeps on COI cannot be discounted); a pattern observed worldwide at vent communities and may reflect demographic instability over time as a consequence of the stochastic birth and death of vent colonies within a metapopulation. Different COI bottleneck ages between the three species (excluding the influence of possible selection) as well as the absence of kiwaids and peltospirids at Kemp, have been attributed to differences in life history, in particular larval morphology and presumed dispersal strategy. These results highlight the role of larval dispersal of vent fauna along active spreading ridges, both in maintaining vent metapopulations across vent colonies prone to stochastic birth and extinction in the short term, but also in the spread of taxa globally and the formation of biogeographic provinces. The likelihood that the three species presented here exist at vents east of the ESR and SSI, prompts further exploration along ridges in the South Atlantic, in order to investigate the effect of the ACC in enhancing gene flow and delineating biogeographic provinces.

Les sources hydrothermales profondes sont des édifices géologiques formés par l’infiltration d’eau de mer dans la croûte océanique, formant un fluide chaud (>400 °C), riche en métaux qui précipite pour former des cheminées dans lesquelles circulent un courant électrique. Les travaux de recherche présentés ici avaient pour objectif de révéler la présence de microorganismes capable de participer à la production de ce courant électrique ou d’utiliser cette électricité pour vivre au sein de ces cheminées électriquement conductrices. Nous nous sommes focalisés sur les microorganismes capables de survivre à haute température (entre 60 et 95°C). Différentes communautés microbienne en interaction et électroactives ont pu être cultivées permettant de poser des hypothèses crédibles quant à la colonisation primaire de ces environnements extrêmes. Ces hypothèses pourraient également s’appliquer aux théories d’origine de la vie en contexte hydrothermal. / Deep hydrothermal vents are geologic structures formed by the infiltration of seawater into the oceanic crust, forming a hot metal-rich fluid (> 400 ° C) that precipitates to form chimneys in which an electric current flows. The purpose of the research presented here was to reveal the presence of microorganisms capable of participating in the production of this electric current or of using this electricity to live within these electrically conductive chimneys. We focused on microorganisms able to survive at high temperatures (between 60 and 95 ° C). Different interacting and electroactive microbial communities have been cultivated, allowing the building of credible hypotheses about the primary colonization of these extreme environments. These hypotheses could also be applied to theories of origin of life in a hydrothermal context.

Les sources hydrothermales océaniques profondes renferment des écosystèmes extrêmes, situés dans la zone abyssale des Océans. Dans ces environnements dépourvus de lumière, la production primaire est réalisée par la chimiosynthèse microbienne. Ces milieux sont colonisés par des espèces animales, dont la plupart vivent en associations plus ou moins fortes avec des micro-organismes. La crevette Rimicaris exoculata est une espèce hydrothermale endémique des sites de la Ride-Médio-Atlantique (MAR), qui domine la plupart des sites qu’elle colonise. Ce crustacé a pour particularité de posséder deux communautés symbiotiques : une située dans son céphalothorax hypertrophié et une inféodée à son tractus digestif. Tout d’abord, ce travail de thèse s’est concentré sur l’étude de la communication bactérienne (Quorum Sensing ou QS) au sein des communautés ectosymbiotiques de R. exoculata au cours de son cycle de mue et de vie. Ensuite, ce travail s’est focalisé sur l’identification d’un peptide antimicrobien (PAM), puis à rechercher sa fonction dans l'immunité et le contrôle des symbiotes chez Rimicaris exoculata. Ce travail a permis, d’une part, de confirmer la présence de deux gènes du QS (luxS et luxR) dans les communautés ectosymbiotiques de R. exoculata sur quatre sites hydrothermaux : Rainbow, TAG, Snake Pit et Logatchev. Ces gènes étant plus divergents que ceux de l'ARNr 16S, leur utilisation comme marqueurs génétiques biogéographiques pour retracer l'origine des individus est discuté. Ce travail a permis, d’autre part, d’identifier pour la première fois un PAM (sus nommé Re-crustin), chez un arthropode hydrothermal. Les données suggèrent une participation de ce PAM dans le contrôle de l’ectosymbiose. L’ensemble de ces travaux apporte de nouvelles hypothèses sur l’interaction entre les épibiontes du céphalothorax et la crevette Rimicaris exoculata. / Deprived of light, the deep-sea hydrothermal vents are extremes ecosystems sustained by micobial chemosynthesis. These environments are colonized by animal species living in close relationships with these chemoautotrophic micro-organisms, eating them or establishing long term interactions with them, may they be trophic or not only. The shrimp Rimicaris exoculata is an endemic hydrothermal species of the Mid-Atlantic Ridge (MAR) sites. This crustacean represents the predominant macrofauna of some sites of the MAR. It lives in symbiotic association with two distinct microbial communities qualified as ectosymbiosis. One is located in its gill chamber and one in its gut. First, this work focused on the study of bacterial communication (Quorum Sensing or QS) within the ectosymbiontic communities during the molting and life cycles of R. exoculata. Then, we focused on an antimicrobial peptide (AMP) identification and search for its function in R. exoculata immunity and in controlling symbionts. Two QS genes (luxS and luxR) were identified in the R. exoculata ectosymbiontic community at different shrimp molt stages and life stages at the Rainbow, TAG, Snake Pit and Logatchev vent sites.As these genes are more divergent than that of 16S rRNA, they could be then used as biogeographical genetic markers tools to trace back the origin of individuals to a location or between locations along its life cycle. This work reports also the first description of an AMP in an extremophile arthropod (namely Recrustin). Data suggest a participation of this AMP in the control of the ectosymbiosis in Rimicarisexoculata. All this work provides new hypotheses wich are discussed in the manuscript, dealing with the interaction between symbionts and Rimicaris exoculata.

Thesis (Ph. D.)--Joint Program in Oceanography/Applied Ocean Science and Engineering (Massachusetts Institute of Technology, Dept. of Biology; and the Woods Hole Oceanographic Institution), 2008. / This electronic version was submitted by the student author. The certified thesis is available in the Institute Archives and Special Collections. / Includes bibliographical references. / Ecological processes at deep-sea hydrothermal vents on fast-spreading mid-ocean ridges are punctuated by frequent physical disturbance. Larval dispersal among disjunct vent sites facilitates the persistence of sessile invertebrate species in these geologically and chemically dynamic habitats despite local extinction events. Regional population extension and rapid recolonization by the siboglinid tubeworm Riftia pachyptila have been well documented along the East Pacific Rise and the Galápagos Rift. To analyze spatial and temporal population genetic patterns and the processes governing them at ephemeral and disjunct habitats, a suite of 12 highly variable microsatellite DNA markers were developed for this species. Eight of these loci were used to assess the regional and within-ridge genetic structure of recent colonists and resident adults collected from nine sites in the eastern Pacific Ocean over period of three to seven years. A significant seafloor eruption during the seven-year sampling period allowed investigation into the role of local extinction in population genetic diversity at the Tica vent site at 9°N EPR, while collections within two and five years of an eruption that created the Rosebud vent field at 86°W GAR provided insights into genetic diversity input over population establishment. For the first time, this thesis demonstrated significant genetic differences between Riftia populations on the East Pacific Rise and Galápagos Rift. Moreover, the separate treatment of colonist and resident subpopulations revealed a high potential for local larval retention at vent sites. This mechanism for recruitment likely sustains disjunct populations and supports the recolonization of locally extinct areas after disturbance events, while episodic long-distance dispersal maintains genetic coherence of the species. / (cont.) Temporal population genetic consideration at the Tica site on the East Pacific Rise suggests that the 2005-2006 seafloor eruption had little to no discernable effect on local population genetic composition. Yet local populations appear to exhibit a small degree of genetic patchiness, with a high degree of relatedness (half-sibs) among subsets of individuals within both colonist and resident cohorts. This thesis broadens the application of recently developed molecular techniques to study the effect of ridge-crest processes and offers new perspectives into marine dispersal, gene flow, and population differentiation. / by Abigail Jean Fusaro. / Ph.D.