skip to main content


Title: Microbial epibiotic community of the deep-sea galatheid squat lobster Munidopsis alvisca
Abstract

Life at hydrothermal vent sites is based on chemosynthetic primary producers that supply heterotrophic microorganisms with substrates and generate biomass for higher trophic levels. Often, chemoautotrophs associate with the hydrothermal vent megafauna. To investigate attached bacterial and archaeal communities on deep-sea squat lobsters, we collected ten specimens from a hydrothermal vent in the Guaymas Basin (Gulf of California). All animals were identified asMunidopsis alviscavia morphological and molecular classification, and intraspecific divergence was determined. Amplicon sequencing of microbial DNA and cDNA revealed significant differences between microbial communities on the carapaces ofM. alviscaand those in ambient sea water. Major epibiotic bacterial taxa were chemoautotrophicGammaproteobacteria, such asThiotrichaceaeandMethylococcaceae, while archaea were almost exclusively represented by sequences affiliated withCa. Nitrosopumilus. In sea water samples, Marine Group II and III archaea and organoheterotrophicAlphaproteobacteria,FlavobacteriiaandPlanctomycetaciawere more dominant. Based on the identified taxa, we assume that main metabolic processes, carried out byM. alviscaepibiota, include ammonia, methane and sulphide oxidation. Considering thatM. alviscacould benefit from sulphide detoxification by its epibiota, and that attached microbes are supplied with a stable habitat in proximity to substrate-rich hydrothermal fluids, a mutualistic host-microbe relationship appears likely.

 
more » « less
NSF-PAR ID:
10362925
Author(s) / Creator(s):
; ; ; ; ; ;
Publisher / Repository:
Nature Publishing Group
Date Published:
Journal Name:
Scientific Reports
Volume:
12
Issue:
1
ISSN:
2045-2322
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Background

    When deep-sea hydrothermal fluids mix with cold oxygenated fluids, minerals precipitate out of solution and form hydrothermal deposits. These actively venting deep-sea hydrothermal deposits support a rich diversity of thermophilic microorganisms which are involved in a range of carbon, sulfur, nitrogen, and hydrogen metabolisms. Global patterns of thermophilic microbial diversity in deep-sea hydrothermal ecosystems have illustrated the strong connectivity between geological processes and microbial colonization, but little is known about the genomic diversity and physiological potential of these novel taxa. Here we explore this genomic diversity in 42 metagenomes from four deep-sea hydrothermal vent fields and a deep-sea volcano collected from 2004 to 2018 and document their potential implications in biogeochemical cycles.

    Results

    Our dataset represents 3635 metagenome-assembled genomes encompassing 511 novel and recently identified genera from deep-sea hydrothermal settings. Some of the novel bacterial (107) and archaeal genera (30) that were recently reported from the deep-sea Brothers volcano were also detected at the deep-sea hydrothermal vent fields, while 99 bacterial and 54 archaeal genera were endemic to the deep-sea Brothers volcano deposits. We report some of the first examples of medium- (≥ 50% complete, ≤ 10% contaminated) to high-quality (> 90% complete, < 5% contaminated) MAGs from phyla and families never previously identified, or poorly sampled, from deep-sea hydrothermal environments. We greatly expand the novel diversity of Thermoproteia, Patescibacteria (Candidate Phyla Radiation, CPR), and Chloroflexota found at deep-sea hydrothermal vents and identify a small sampling of two potentially novel phyla, designated JALSQH01 and JALWCF01. Metabolic pathway analysis of metagenomes provides insights into the prevalent carbon, nitrogen, sulfur, and hydrogen metabolic processes across all sites and illustrates sulfur and nitrogen metabolic “handoffs” in community interactions. We confirm that Campylobacteria and Gammaproteobacteria occupy similar ecological guilds but their prevalence in a particular site is driven by shifts in the geochemical environment.

    Conclusion

    Our study of globally distributed hydrothermal vent deposits provides a significant expansion of microbial genomic diversity associated with hydrothermal vent deposits and highlights the metabolic adaptation of taxonomic guilds. Collectively, our results illustrate the importance of comparative biodiversity studies in establishing patterns of shared phylogenetic diversity and physiological ecology, while providing many targets for enrichment and cultivation of novel and endemic taxa.

     
    more » « less
  2. Shallow water hydrothermal vents represent highly dynamic environments where strong geochemical gradients can shape microbial communities. Recently, these systems are being widely used for investigating the effects of ocean acidification on biota as vent emissions can release high CO 2 concentrations causing local pH reduction. However, other gas species, as well as trace elements and metals, are often released in association with CO 2 and can potentially act as confounding factors. In this study, we evaluated the composition, diversity and inferred functional profiles of microbial biofilms in Levante Bay (Vulcano Island, Italy, Mediterranean Sea), a well-studied shallow-water hydrothermal vent system. We analyzed 16S rRNA transcripts from biofilms exposed to different intensity of hydrothermal activity, following a redox and pH gradient across the bay. We found that elevated CO 2 concentrations causing low pH can affect the response of bacterial groups and taxa by either increasing or decreasing their relative abundance. H 2 S proved to be a highly selective factor shaping the composition and affecting the diversity of the community by selecting for sulfide-dependent, chemolithoautotrophic bacteria. The analysis of the 16S rRNA transcripts, along with the inferred functional profile of the communities, revealed a strong influence of H 2 S in the southern portion of the study area, and temporal succession affected the inferred abundance of genes for key metabolic pathways. Our results revealed that the composition of the microbial assemblages vary at very small spatial scales, mirroring the highly variable geochemical signature of vent emissions and cautioning for the use of these environments as models to investigate the effects of ocean acidification on microbial diversity. 
    more » « less
  3. Abstract

    Current methods for biochemical and biogeochemical analysis of the deep-sea hydrothermal vent ecosystems rely on water sample recovery, orin situanalysis using underwater instruments with limited range of analyte detection and limited sensitivity. Even in cases where large quantities of sample are recovered, labile dissolved organic compounds may not be detected due to time delays between sampling and preservation. Here, we present a novel approach forin situextraction of organic compounds from hydrothermal vent fluids through a unique solid phase microextraction (SPME) sampler. These samplers were deployed to sample effluent of vents on sulphide chimneys, located on Axial Seamount in the North-East Pacific, in the Urashima field on the southern Mariana back-arc, and at the Hafa Adai site in the central Mariana back-arc. Among the compounds that were extracted, a wide range of unique organic compounds, including labile dissolved organic sulfur compounds, were detected through high-resolution LC-MS/MS, among which were biomarkers of anammox bacteria, fungi, and lower animals. This report is the first to show that SPME can contribute to a broader understanding of deep sea ecology and biogeochemical cycles in hydrothermal vent ecosystems.

     
    more » « less
  4. Chi Fru, Ernest ; Chik, Alex ; Colwell, Fredrick ; Dittrich, Maria ; Engel, Annette ; Keenan, Sarah ; Meckenstock, Rainer ; Omelon, Christopher ; Purkamo, Lotta ; Weisener, Chris (Ed.)

    Roots are common features in basaltic lava tube caves on the island of Hawai‘i. For the past 50 years, new species of cave-adapted invertebrates, including cixiid planthoppers, crickets, thread-legged bugs, and spiders, have been discovered from root patches in lava tubes on different volcanoes and across variable climatic conditions. Assessing vegetation on the surface above lava tube passages, as well as genetic characterization of roots from within lava tubes, suggest that most roots belong to the native pioneer tree, ‘ōhi‘a lehua (Metrosideros polymorpha). Planthoppers are the primary consumers of sap at the base of the subsurface food web. However, root physicochemistry and rhizobiome microbial diversity and functional potential have received little attention. This study focuses on characterizing the ‘ōhi‘a rhizobiome, accessed from free-hanging roots inside lava tubes. Using these results, we can begin to evaluate the development and evolution of plant-microbe-invertebrate relationships.

    We explored lava tubes formed in flows of differing elevations and ages, from about 140 to 3000 years old, on Mauna Loa, Kīlauea, and Hualālai volcanoes on Hawai‘i Island. Invertebrate diversity was evaluated from root galleries and non-root galleries, in situ fluid physicochemistry was measured, and root and bare rock fluids (e.g., water, sap) were collected to determine major ion concentrations, as well as non-purgeable organic carbon (NPOC) and total nitrogen (TN) content. To verify root identity, DNA was extracted, and three sets of primers were used. After screening for onlyMetrosiderosspp., the V4 region of the 16S rRNA gene was sequenced and taxonomy was assigned.

    Root fluids were viscous and ranged in color from clear to yellow to reddish orange. Root fluids had 2X to 10X higher major ion concentrations compared to rock water. The average root NPOC and TN concentrations were 192 mg/L and 5.2 mg/L, respectively, compared to rock water that had concentrations of 6.8 mg/L and 1.8 mg/L, respectively. Fluids from almost 300 root samples had pH values that ranged from 2.2 to 5.6 (average pH 4.63) and were lower than rock water (average pH 6.39). Root fluid pH was comparable to soil pH from montane wet forests dominated by ‘ōhi‘a (Selmants et al. 2016), which can grow in infertile soil with pH values as low as 3.6. On Hawai‘i, rain water pH averages 5.2 at sea level and systematically decreases with elevation to pH 4.3 at 2500 m (Miller and Yoshinaga 2012), but root fluid pH did not correlate with elevation, temperature, relative humidity, inorganic and organic constituents, or age of flow. Root fluid acidity is likely due to concentrated organic compounds, sourced as root exudates, and this habitat is acidic for the associated invertebrates.

    From 62 root samples, over 66% were identified to the genusMetrosideros. A few other identifications of roots from lava tube systems where there had been extensive clear-cutting and ranching included monkey pod tree, coconut palm,Ficusspp., and silky oak.

    The 16S rRNA gene sequence surveys revealed that root bacterial communities were dominated by few groups, including Burkholderiaceae, as well as Acetobacteraceae, Sphingomonadaceae, Acidobacteriaceae, Gemmataceae, Xanthobacteraceae, and Chitinophagaceae. However, most of the reads could not be classified to a specific genus, which suggested that the rhizobiome harbor novel diversity. Diversity was higher from wetter climates. The root communities were distinct from those described previously from ‘ōhi‘a flowers and leaves (Junker and Keller 2015) and lava tube rocky surfaces (Hathaway et al. 2014) where microbial groups were specifically presumed capable of heterotrophy, methanotrophy, diazotrophy, and nitrification. Less can be inferred for the rhizobiome metabolism, although most taxa are likely aerobic heterotrophs. Within the Burkholderiaceae, there were high relative abundances of sequences affiliated with the genusParaburkholderia, which includes known plant symbionts, as well as the acidophilic generaAcidocellaandAcidisomafrom the Acetobacteraceae, which were retrieved predominately from caves in the oldest lava flows that also had the lowest root pH values. It is likely that the bacterial groups are capable of degrading exudates and providing nutritional substrates for invertebrate consumers that are not provided by root fluids (i.e., phloem) alone.

    As details about the biochemistry of ‘ōhi‘a have been missing, characterizing the rhizobiome from lava tubes will help to better understand potential plant-microbe-invertebrate interactions and ecological and evolutionary relationships through time. In particular, the microbial rhizobiome may produce compounds used by invertebrates nutritionally or that affect their behavior, and changes to the rhizobiome in response to environmental conditions may influence invertebrate interactions with the roots, which could be important to combat climate change effects or invasive species introductions.

     
    more » « less
  5. Giovannoni, Stephen J. (Ed.)
    ABSTRACT <p>Archaea belonging to the DPANN (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, and Nanohaloarchaeota) superphylum have been found in an expanding number of environments and perform a variety of biogeochemical roles, including contributing to carbon, sulfur, and nitrogen cycling. Generally characterized by ultrasmall cell sizes and reduced genomes, DPANN archaea may form mutualistic, commensal, or parasitic interactions with various archaeal and bacterial hosts, influencing the ecology and functioning of microbial communities. While DPANN archaea reportedly comprise a sizeable fraction of the archaeal community within marine oxygen-deficient zone (ODZ) water columns, little is known about their metabolic capabilities in these ecosystems. We report 33 novel metagenome-assembled genomes (MAGs) belonging to the DPANN phyla Nanoarchaeota, Pacearchaeota, Woesearchaeota, Undinarchaeota, Iainarchaeota, and SpSt-1190 from pelagic ODZs in the Eastern Tropical North Pacific and the Arabian Sea. We find these archaea to be permanent, stable residents of all three major ODZs only within anoxic depths, comprising up to 1% of the total microbial community and up to 25%–50% of archaea as estimated from read mapping to MAGs. ODZ DPANN appear to be capable of diverse metabolic functions, including fermentation, organic carbon scavenging, and the cycling of sulfur, hydrogen, and methane. Within a majority of ODZ DPANN, we identify a gene homologous to nitrous oxide reductase. Modeling analyses indicate the feasibility of a nitrous oxide reduction metabolism for host-attached symbionts, and the small genome sizes and reduced metabolic capabilities of most DPANN MAGs suggest host-associated lifestyles within ODZs.</p></sec> <sec><title>IMPORTANCE

    Archaea from the DPANN (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, and Nanohaloarchaeota) superphylum have diverse metabolic capabilities and participate in multiple biogeochemical cycles. While metagenomics and enrichments have revealed that many DPANN are characterized by ultrasmall genomes, few biosynthetic genes, and episymbiotic lifestyles, much remains unknown about their biology. We report 33 new DPANN metagenome-assembled genomes originating from the three global marine oxygen-deficient zones (ODZs), the first from these regions. We survey DPANN abundance and distribution within the ODZ water column, investigate their biosynthetic capabilities, and report potential roles in the cycling of organic carbon, methane, and nitrogen. We test the hypothesis that nitrous oxide reductases found within several ODZ DPANN genomes may enable ultrasmall episymbionts to serve as nitrous oxide consumers when attached to a host nitrous oxide producer. Our results indicate DPANN archaea as ubiquitous residents within the anoxic core of ODZs with the potential to produce or consume key compounds.

     
    more » « less