Anderson
Rika E.
Anderson
Rika E.
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ArticleSelection is a significant driver of gene gain and loss in the pangenome of the bacterial genus Sulfurovum in geographically distinct deep-sea hydrothermal vents(American Society for Microbiology, 2020-04-14) Moulana, Alief ; Anderson, Rika E. ; Fortunato, Caroline S. ; Huber, Julie A.Microbial genomes have highly variable gene content, and the evolutionary history of microbial populations is shaped by gene gain and loss mediated by horizontal gene transfer and selection. To evaluate the influence of selection on gene content variation in hydrothermal vent microbial populations, we examined 22 metagenome-assembled genomes (MAGs) (70 to 97% complete) from the ubiquitous vent Epsilonbacteraeota genus Sulfurovum that were recovered from two deep-sea hydrothermal vent regions, Axial Seamount in the northeastern Pacific Ocean (13 MAGs) and the Mid-Cayman Rise in the Caribbean Sea (9 MAGs). Genes involved in housekeeping functions were highly conserved across Sulfurovum lineages. However, genes involved in environment-specific functions, and in particular phosphate regulation, were found mostly in Sulfurovum genomes from the Mid-Cayman Rise in the low-phosphate Atlantic Ocean environment, suggesting that nutrient limitation is an important selective pressure for these bacteria. Furthermore, genes that were rare within the pangenome were more likely to undergo positive selection than genes that were highly conserved in the pangenome, and they also appeared to have experienced gene-specific sweeps. Our results suggest that selection is a significant driver of gene gain and loss for dominant microbial lineages in hydrothermal vents and highlight the importance of factors like nutrient limitation in driving microbial adaptation and evolution.
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ArticleMetabolic strategies shared by basement residents of the lost city hydrothermal field(American Society for Microbiology, 2022-09-13) Brazelton, William J. ; McGonigle, Julia M. ; Motamedi, Shahrzad ; Pendleton, H. Lizethe ; Twing, Katrina I. ; Miller, Briggs C. ; Lowe, William J. ; Hoffman, Alessandrina M. ; Prator, Cecilia A. ; Chadwick, Grayson L. ; Anderson, Rika E. ; Thomas, Elaina ; Butterfield, David A. ; Aquino, Karmina A. ; Fruh-Green, Gretchen L. ; Schrenk, Matthew O. ; Lang, Susan Q.Alkaline fluids venting from chimneys of the Lost City hydrothermal field flow from a potentially vast microbial habitat within the seafloor where energy and organic molecules are released by chemical reactions within rocks uplifted from Earth’s mantle. In this study, we investigated hydrothermal fluids venting from Lost City chimneys as windows into subseafloor environments where the products of geochemical reactions, such as molecular hydrogen (H2), formate, and methane, may be the only available sources of energy for biological activity. Our deep sequencing of metagenomes and metatranscriptomes from these hydrothermal fluids revealed a few key species of archaea and bacteria that are likely to play critical roles in the subseafloor microbial ecosystem. We identified a population of Thermodesulfovibrionales (belonging to phylum Nitrospirota) as a prevalent sulfate-reducing bacterium that may be responsible for much of the consumption of H2 and sulfate in Lost City fluids. Metagenome-assembled genomes (MAGs) classified as Methanosarcinaceae and Candidatus Bipolaricaulota were also recovered from venting fluids and represent potential methanogenic and acetogenic members of the subseafloor ecosystem. These genomes share novel hydrogenases and formate dehydrogenase-like sequences that may be unique to hydrothermal environments where H2 and formate are much more abundant than carbon dioxide. The results of this study include multiple examples of metabolic strategies that appear to be advantageous in hydrothermal and subsurface alkaline environments where energy and carbon are provided by geochemical reactions.
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ArticleHeterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru(National Academy of Sciences, 2006-02-27) Biddle, Jennifer F. ; Lipp, Julius S. ; Lever, Mark A. ; Lloyd, Karen G. ; Sorensen, Ketil B. ; Anderson, Rika E. ; Fredricks, Helen F. ; Elvert, Marcus ; Kelly, Timothy J. ; Schrag, Daniel P. ; Sogin, Mitchell L. ; Brenchley, Jean E. ; Teske, Andreas ; House, Christopher H. ; Hinrichs, Kai-UweStudies of deeply buried, sedimentary microbial communities and associated biogeochemical processes during Ocean Drilling Program Leg 201 showed elevated prokaryotic cell numbers in sediment layers where methane is consumed anaerobically at the expense of sulfate. Here, we show that extractable archaeal rRNA, selecting only for active community members in these ecosystems, is dominated by sequences of uncultivated Archaea affiliated with the Marine Benthic Group B and the Miscellaneous Crenarchaeotal Group, whereas known methanotrophic Archaea are not detectable. Carbon flow reconstructions based on stable isotopic compositions of whole archaeal cells, intact archaeal membrane lipids, and other sedimentary carbon pools indicate that these Archaea assimilate sedimentary organic compounds other than methane even though methanotrophy accounts for a major fraction of carbon cycled in these ecosystems. Oxidation of methane by members of Marine Benthic Group B and the Miscellaneous Crenarchaeotal Group without assimilation of methane–carbon provides a plausible explanation. Maintenance energies of these subsurface communities appear to be orders of magnitude lower than minimum values known from laboratory observations, and ecosystem-level carbon budgets suggest that community turnover times are on the order of 100–2,000 years. Our study provides clues about the metabolic functionality of two cosmopolitan groups of uncultured Archaea.
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ArticleDiverse viruses in deep-sea hydrothermal vent fluids have restricted dispersal across ocean basins(American Society for Microbiology, 2021-06-22) Thomas, Elaina ; Anderson, Rika E. ; Li, Viola ; Rogan, L. Jenni ; Huber, Julie A.In the ocean, viruses impact microbial mortality, regulate biogeochemical cycling, and alter the metabolic potential of microbial lineages. At deep-sea hydrothermal vents, abundant viruses infect a wide range of hosts among the archaea and bacteria that inhabit these dynamic habitats. However, little is known about viral diversity, host range, and biogeography across different vent ecosystems, which has important implications for how viruses manipulate microbial function and evolution. Here, we examined viral diversity, viral and host distribution, and virus-host interactions in microbial metagenomes generated from venting fluids from several vent sites within three different geochemically and geographically distinct hydrothermal systems: Piccard and Von Damm vent fields at the Mid-Cayman Rise in the Caribbean Sea, and at several vent sites within Axial Seamount in the Pacific Ocean. Analysis of viral sequences and clustered regularly interspaced short palindromic repeat (CRISPR) spacers revealed highly diverse viral assemblages and evidence of active infection. Network analysis revealed that viral host range was relatively narrow, with very few viruses infecting multiple microbial lineages. Viruses were largely endemic to individual vent sites, indicating restricted dispersal, and in some cases, viral assemblages persisted over time. Thus, we show that hydrothermal vent fluids are home to novel, diverse viral assemblages that are highly localized to specific regions and taxa.
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ArticleGenomic variation in microbial populations inhabiting the marine subseafloor at deep-sea hydrothermal vents(Nature Publishing Group, 2017-10-24) Anderson, Rika E. ; Reveillaud, Julie ; Reddington, Emily ; Delmont, Tom O. ; Eren, A. Murat ; McDermott, Jill M. ; Seewald, Jeffrey S. ; Huber, Julie A.Little is known about evolutionary drivers of microbial populations in the warm subseafloor of deep-sea hydrothermal vents. Here we reconstruct 73 metagenome-assembled genomes (MAGs) from two geochemically distinct vent fields in the Mid-Cayman Rise to investigate patterns of genomic variation within subseafloor populations. Low-abundance populations with high intra-population diversity coexist alongside high-abundance populations with low genomic diversity, with taxonomic differences in patterns of genomic variation between the mafic Piccard and ultramafic Von Damm vent fields. Populations from Piccard are significantly enriched in nonsynonymous mutations, suggesting stronger purifying selection in Von Damm relative to Piccard. Comparison of nine Sulfurovum MAGs reveals two high-coverage, low-diversity MAGs from Piccard enriched in unique genes related to the cellular membrane, suggesting these populations were subject to distinct evolutionary pressures that may correlate with genes related to nutrient uptake, biofilm formation, or viral invasion. These results are consistent with distinct evolutionary histories between geochemically different vent fields, with implications for understanding evolutionary processes in subseafloor microbial populations.
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ArticleEvolutionary strategies of viruses, bacteria and archaea in hydrothermal vent ecosystems revealed through metagenomics(Public Library of Science, 2014-10-03) Anderson, Rika E. ; Sogin, Mitchell L. ; Baross, John A.The deep-sea hydrothermal vent habitat hosts a diverse community of archaea and bacteria that withstand extreme fluctuations in environmental conditions. Abundant viruses in these systems, a high proportion of which are lysogenic, must also withstand these environmental extremes. Here, we explore the evolutionary strategies of both microorganisms and viruses in hydrothermal systems through comparative analysis of a cellular and viral metagenome, collected by size fractionation of high temperature fluids from a diffuse flow hydrothermal vent. We detected a high enrichment of mobile elements and proviruses in the cellular fraction relative to microorganisms in other environments. We observed a relatively high abundance of genes related to energy metabolism as well as cofactors and vitamins in the viral fraction compared to the cellular fraction, which suggest encoding of auxiliary metabolic genes on viral genomes. Moreover, the observation of stronger purifying selection in the viral versus cellular gene pool suggests viral strategies that promote prolonged host integration. Our results demonstrate that there is great potential for hydrothermal vent viruses to integrate into hosts, facilitate horizontal gene transfer, and express or transfer genes that manipulate the hosts’ functional capabilities.
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PreprintBiogeography and ecology of the rare and abundant microbial lineages in deep-sea hydrothermal vents( 2014-11) Anderson, Rika E. ; Sogin, Mitchell L. ; Baross, John A.Environmental gradients generate countless ecological niches in deep-sea hydrothermal vent systems, which foster diverse microbial communities. The majority of distinct microbial lineages in these communities occur in very low abundance. However, the ecological role and distribution of rare and abundant lineages, particularly in deep, hot subsurface environments, remains unclear. Here, we use 16S rRNA tag sequencing to describe biogeographic patterning and microbial community structure of both rare and abundant archaea and bacteria in hydrothermal vent systems. We show that while rare archaeal lineages and almost all bacterial lineages displayed geographically restricted community structuring patterns, the abundant lineages of archaeal communities displayed a much more cosmopolitan distribution. Finally, analysis of one high-volume, high-temperature fluid sample representative of the deep hot biosphere described a unique microbial community that differed from microbial populations in diffuse flow fluid or sulfide samples, yet the rare thermophilic archaeal groups showed similarities to those that occur in sulfides. These results suggest that while most archaeal and bacterial lineages in vents are rare and display a highly regional distribution, a small percentage of lineages, particularly within the archaeal domain, are successful at widespread dispersal and colonization.
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ArticleNew opportunities and untapped scientific potential in the abyssal ocean(Frontiers Media, 2022-02-03) Marlow, Jeffrey ; Anderson, Rika E. ; Reysenbach, Anna-Louise ; Seewald, Jeffrey S. ; Shank, Timothy M. ; Teske, Andreas P. ; Wanless, V. Dorsey ; Soule, S. AdamThe abyssal ocean covers more than half of the Earth’s surface, yet remains understudied and underappreciated. In this Perspectives article, we mark the occasion of the Deep Submergence Vehicle Alvin’s increased depth range (from 4500 to 6500 m) to highlight the scientific potential of the abyssal seafloor. From a geologic perspective, ultra-slow spreading mid-ocean ridges, Petit Spot volcanism, transform faults, and subduction zones put the full life cycle of oceanic crust on display in the abyss, revealing constructive and destructive forces over wide ranges in time and space. Geochemically, the abyssal pressure regime influences the solubility of constituents such as silica and carbonate, and extremely high-temperature fluid-rock reactions in the shallow subsurface lead to distinctive and potentially unique geochemical profiles. Microbial residents range from low-abundance, low-energy communities on the abyssal plains to fast growing thermophiles at hydrothermal vents. Given its spatial extent and position as an intermediate zone between coastal and deep hadal settings, the abyss represents a lynchpin in global-scale processes such as nutrient and energy flux, population structure, and biogeographic diversity. Taken together, the abyssal ocean contributes critical ecosystem services while facing acute and diffuse anthropogenic threats from deep-sea mining, pollution, and climate change.
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ArticleMetagenomic investigation of vestimentiferan tubeworm endosymbionts from Mid-Cayman Rise reveals new insights into metabolism and diversity(BMC, 2018-01-27) Reveillaud, Julie ; Anderson, Rika E. ; Reves-Sohn, Sintra ; Cavanaugh, Colleen M. ; Huber, Julie A.The microbial endosymbionts of two species of vestimentiferan tubeworms (Escarpia sp. and Lamellibrachia sp.2) collected from an area of low-temperature hydrothermal diffuse vent flow at the Mid-Cayman Rise (MCR) in the Caribbean Sea were characterized using microscopy, phylogenetic analyses, and a metagenomic approach. Bacteria, with a typical Gram negative cell envelope contained within membrane-bound vacuoles, were observed within the trophosome of both tubeworm species. Phylogenetic analysis of the 16S rRNA gene and ITS region suggested MCR individuals harbored highly similar endosymbionts that were > 98% identical, with the exception of two symbionts that showed a 60 bp insertion within the ITS region. All sequences from MCR endosymbionts formed a separate well-supported clade that diverged from those of symbionts of seep and vent vestimentiferans from the Pacific, Gulf of Mexico, and Mediterranean Sea. The metagenomes of the symbionts of two specimens of each tubeworm species were sequenced, and two distinct Gammaproteobacteria metagenome-assembled genomes (MAGs) of more than 4 Mbp assembled. An Average Nucleotide Identity (ANI) of 86.5% between these MAGs, together with distinct 16S rRNA gene and ITS sequences, indicate the presence of multiple endosymbiont phylotypes at the MCR, with one MAG shared between one Escarpia and two Lamellibrachia individuals, indicating these endosymbionts are not specific to either host species. Genes for sulfur and hydrogen oxidation, nitrate reduction (assimilatory and dissimilatory), glycolysis and the Krebs cycle, peptide, sugar, and lipid transporters, and both rTCA and CBB carbon fixation cycles were detected in the MAGs, highlighting key and shared functions with symbiont metagenomes of the vestimentiferans Riftia, Tevnia, and Ridgeia from the Pacific. The potential for a second hydrogen oxidation pathway (via a bidirectional hydrogenase), formate dehydrogenase, a catalase, and several additional peptide transporters were found exclusively in the MCR endosymbiont MAGs. The present study adds new evidence that tubeworm endosymbionts can potentially switch from autotrophic to heterotrophic metabolism, or may be mixotrophic, presumably while free-living, and also suggests their versatile metabolic potential may enable both the host and symbionts to exploit a wide range of environmental conditions. Together, the marked gene content and sequence dissimilarity at the rRNA operon and whole genome level between vent and seep symbionts suggest these newly described endosymbionts from the MCR belong to a novel tubeworm endosymbiont genera, introduced as Candidatus Vondammii.
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ArticleMicrobial populations are shaped by dispersal and recombination in a low biomass subseafloor habitat(American Society for Microbiology, 2022-08-01) Anderson, Rika E. ; Graham, Elaina D. ; Huber, Julie A. ; Tully, Benjamin J.The subseafloor is a vast habitat that supports microorganisms that have a global scale impact on geochemical cycles. Many of the endemic microbial communities inhabiting the subseafloor consist of small populations under growth-limited conditions. For small populations, stochastic evolutionary events can have large impacts on intraspecific population dynamics and allele frequencies. These conditions are fundamentally different from those experienced by most microorganisms in surface environments, and it is unknown how small population sizes and growth-limiting conditions influence evolution and population structure in the subsurface. Using a 2-year, high-resolution environmental time series, we examine the dynamics of microbial populations from cold, oxic crustal fluids collected from the subseafloor site North Pond, located near the mid-Atlantic ridge. Our results reveal rapid shifts in overall abundance, allele frequency, and strain abundance across the time points observed, with evidence for homologous recombination between coexisting lineages. We show that the subseafloor aquifer is a dynamic habitat that hosts microbial metapopulations that disperse frequently through the crustal fluids, enabling gene flow and recombination between microbial populations. The dynamism and stochasticity of microbial population dynamics in North Pond suggest that these forces are important drivers in the evolution of microbial populations in the vast subseafloor habitat.
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ArticleMicrobial eukaryotic predation pressure and biomass at deep-sea hydrothermal vents(Oxford University Press, 2024-01-13) Hu, Sarah K. ; Anderson, Rika E. ; Pachiadaki, Maria G. ; Edgcomb, Virginia P. ; Serres, Margrethe H. ; Sylva, Sean P. ; German, Christopher R. ; Seewald, Jeffrey S. ; Lang, Susan Q. ; Huber, Julie A.Deep-sea hydrothermal vent geochemistry shapes the foundation of the microbial food web by fueling chemolithoautotrophic microbial activity. Microbial eukaryotes (or protists) play a critical role in hydrothermal vent food webs as consumers and hosts of symbiotic bacteria, and as a nutritional source to higher trophic levels. We measured microbial eukaryotic cell abundance and predation pressure in low-temperature diffuse hydrothermal fluids at the Von Damm and Piccard vent fields along the Mid-Cayman Rise in the Western Caribbean Sea. We present findings from experiments performed under in situ pressure that show cell abundances and grazing rates higher than those done at 1 atmosphere (shipboard ambient pressure); this trend was attributed to the impact of depressurization on cell integrity. A relationship between the protistan grazing rate, prey cell abundance, and temperature of end-member hydrothermal vent fluid was observed at both vent fields, regardless of experimental approach. Our results show substantial protistan biomass at hydrothermally fueled microbial food webs, and when coupled with improved grazing estimates, suggest an important contribution of grazers to the local carbon export and supply of nutrient resources to the deep ocean.