The Role of Marine Sponges in Carbon and Nitrogen Cycles of Coral Reef and Nearshore Environments

Sponges and their microbial consortia can alter the water quality of the surrounding environment through animal and hosted microbial chemical transformations resulting from their dynamic pumping, water filtration, and respiration processes. The goal of this dissertation was to quantify the role of these organisms in the cycles of carbon (C) and nitrogen (N) on reefs and representative environments of Florida Bay and describes five principle findings: 1) the abundant coral reef sponge Xestospongia muta satisfies the bulk of its respiration oxygen (O2) demand through uptake of dissolved organic carbon, and this species removed C in excess of O2 demand which is presumed to be reserved for cellular maintenance, growth, and the generation of reproductive materials. 2) Respiration activities in this species yielded a tremendous flux of dissolved inorganic nitrogen (DIN), and the rate of this N release appeared to be broadly conserved between Floridian and Bahamian reefs. 3) The magnitude and speciation of exhalent DIN from species tested in Florida Bay showed similar rates of N efflux as those on the reef, yet the remineralization of particulate organic matter appears to be the dominant feedstock for the observed N release. 4) The N released from these species represented a dominant source of N to a budget calculated for an offshore basin in Florida Bay (Mystery Basin). 5) Bloom conditions swept through Mystery Basin decimating sponge populations and water column N, and yielded significant and lasting changes to the chemical and ecological structure of the system. These results indicated that sponges have the capacity to alter local water quality through the observed C and N transformations mediated by the holobiont (sponge and associated microbiome), and further suggests that they can drastically impact ecosystems where their populations dominate.Doctor of Philosoph

Microbial communities under distinct thermal and geochemical regimes in axial and off-axis sediments of Guaymas Basin

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Teske, A., Wegener, G., Chanton, J. P., White, D., MacGregor, B., Hoer, D., de Beer, D., Zhuang, G., Saxton, M. A., Joye, S. B., Lizarralde, D., Soule, S. A., & Ruff, S. E. Microbial communities under distinct thermal and geochemical regimes in axial and off-axis sediments of Guaymas Basin. Frontiers in Microbiology, 12, (2021): 633649, https://doi.org/10.3389/fmicb.2021.633649.Cold seeps and hydrothermal vents are seafloor habitats fueled by subsurface energy sources. Both habitat types coexist in Guaymas Basin in the Gulf of California, providing an opportunity to compare microbial communities with distinct physiologies adapted to different thermal regimes. Hydrothermally active sites in the southern Guaymas Basin axial valley, and cold seep sites at Octopus Mound, a carbonate mound with abundant methanotrophic cold seep fauna at the Central Seep location on the northern off-axis flanking regions, show consistent geochemical and microbial differences between hot, temperate, cold seep, and background sites. The changing microbial actors include autotrophic and heterotrophic bacterial and archaeal lineages that catalyze sulfur, nitrogen, and methane cycling, organic matter degradation, and hydrocarbon oxidation. Thermal, biogeochemical, and microbiological characteristics of the sampling locations indicate that sediment thermal regime and seep-derived or hydrothermal energy sources structure the microbial communities at the sediment surface.Research on Guaymas Basin in the Teske lab is supported by NSF Molecular and cellular Biology grant 1817381 “Collaborative Research: Next generation physiology: a systems-level understanding of microbes driving carbon cycling in marine sediments”. Sampling in Guaymas Basin was supported by collaborative NSF Biological Oceanography grants 1357238 and 1357360 “Collaborative Research: Microbial carbon cycling and its interaction with sulfur and nitrogen transformations in Guaymas Basin hydrothermal sediments” to AT and SJ, respectively. SER was supported by an AITF/Eyes High Postdoctoral Fellowship and start-up funds provided by the Marine Biological Laboratory

Carbonate-hosted microbial communities are prolific and pervasive methane oxidizers at geologically diverse marine methane seep sites

At marine methane seeps, vast quantities of methane move through the shallow subseafloor, where it is largely consumed by microbial communities. This process plays an important role in global methane dynamics, but we have yet to identify all of the methane sinks in the deep sea. Here, we conducted a continental-scale survey of seven geologically diverse seafloor seeps and found that carbonate rocks from all sites host methane-oxidizing microbial communities with substantial methanotrophic potential. In laboratory-based mesocosm incubations, chimney-like carbonates from the newly described Point Dume seep off the coast of Southern California exhibited the highest rates of anaerobic methane oxidation measured to date. After a thorough analysis of physicochemical, electrical, and biological factors, we attribute this substantial metabolic activity largely to higher cell density, mineral composition, kinetic parameters including an elevated Vmax, and the presence of specific microbial lineages. Our data also suggest that other features, such as electrical conductance, rock particle size, and microbial community alpha diversity, may influence a sample's methanotrophic potential, but these factors did not demonstrate clear patterns with respect to methane oxidation rates. Based on the apparent pervasiveness within seep carbonates of microbial communities capable of performing anaerobic oxidation of methane, as well as the frequent occurrence of carbonates at seeps, we suggest that rock-hosted methanotrophy may be an important contributor to marine methane consumption.https://www.pnas.org/content/118/25/e200685711

Spatial heterogeneity and underlying geochemistry of phylogenetically diverse orange and white Beggiatoa mats in Guaymas Basin hydrothermal sediments

Sulfide-oxidizing bacteria of the genus Beggiatoa are found in conspicuous, colorful mats on the seafloor above active hydrothermal seeps at Guaymas Basin. Guaymas Beggiatoa filaments fall into discrete size classes representing at least five separate 16S rRNA phylotypes, and appear either white, yellow, or orange. During two R/V Atlantis cruises to Guaymas Basin, 78 temperature profiles were taken near and within 15 different orange and white Beggiatoa mats by the Alvin submersible to investigate spatial relationships between mat color and hydrothermal fluid seeps, as indicated by elevated temperatures. The surface temperatures from 78 profiles are similar to each other (on average 8–12 °C, warmer than bare sediments at 3–4 °C), indicating that Guaymas Basin Beggiatoa spp., although relying on the hydrothermal system for energy and carbon sources, live within a relatively cool temperature range. Temperatures from 40 cm below orange Beggiatoa versus white Beggiatoa are the same, at 84 °C averaged across all mat systems. However, within a single mat system, temperatures are higher beneath the predominantly orange center of the mat than beneath the white mat periphery. Push core transects across the orange-to-white color change of three Beggiatoa mats showed stronger upward compression of isotherms and metabolic zones beneath the orange mat center than beneath white mat periphery. Hydrothermal temperature gradients push the microbial processes generating carbon and energy sources for Beggiatoa mats towards the sediment surface. The resulting steep gradients of hydrothermal electron donors and carbon sources to the sediment surface, rather than the in situ temperature by itself, control the relative positioning of orange and white filaments within a Guaymas Basin Beggiatoa mat. Given the wide spectrum of temperature and hydrothermal flux regimes between different mats, the orange/white pattern represents a relative preference or even a competitive balance among different Beggiatoa types that establishes itself within each hydrothermal hot spot. http://dx.doi.org/10.1016/j.dsr.2012.04.01

Carbonate-hosted microbial communities are prolific and pervasive methane oxidizers at geologically diverse marine methane seep sites.

At marine methane seeps, vast quantities of methane move through the shallow subseafloor, where it is largely consumed by microbial communities. This process plays an important role in global methane dynamics, but we have yet to identify all of the methane sinks in the deep sea. Here, we conducted a continental-scale survey of seven geologically diverse seafloor seeps and found that carbonate rocks from all sites host methane-oxidizing microbial communities with substantial methanotrophic potential. In laboratory-based mesocosm incubations, chimney-like carbonates from the newly described Point Dume seep off the coast of Southern California exhibited the highest rates of anaerobic methane oxidation measured to date. After a thorough analysis of physicochemical, electrical, and biological factors, we attribute this substantial metabolic activity largely to higher cell density, mineral composition, kinetic parameters including an elevated Vmax, and the presence of specific microbial lineages. Our data also suggest that other features, such as electrical conductance, rock particle size, and microbial community alpha diversity, may influence a sample's methanotrophic potential, but these factors did not demonstrate clear patterns with respect to methane oxidation rates. Based on the apparent pervasiveness within seep carbonates of microbial communities capable of performing anaerobic oxidation of methane, as well as the frequent occurrence of carbonates at seeps, we suggest that rock-hosted methanotrophy may be an important contributor to marine methane consumption

The Guaymas Basin Hiking Guide to Hydrothermal Mounds, Chimneys, and Microbial Mats: Complex Seafloor Expressions of Subsurface Hydrothermal Circulation

Publisher's PDFThe hydrothermal mats, mounds, and chimneys of the southern Guaymas Basin are the surface expression of complex subsurface hydrothermal circulation patterns. In this overview, we document the most frequently visited features of this hydrothermal area with photographs, temperature measurements, and selected geochemical data; many of these distinct habitats await characterization of their microbial communities and activities. Microprofiler deployments on microbial mats and hydrothermal sediments show their steep geochemical and thermal gradients at millimeter-scale vertical resolution. Mapping these hydrothermal features and sampling locations within the southern Guaymas Basin suggest linkages to underlying shallow sills and heat flow gradients. Recognizing the inherent spatial limitations of much current Guaymas Basin sampling calls for comprehensive surveys of the wider spreading region.University of Delaware, School of Marine Science and Polic

Reduced expression of mitochondrial heavy strand transcripts in m.547A>T patient-derived cells.

<p>(A, C) RNA from patient- and control-derived cells (n = 4 each) was analysed for expression of a panel of mitochondrial tRNAs by quantitative Northern blot. The graphs show mean expression of heavy strand tRNAs relative to light strand tRNA Gln(Q). Values are expressed relative to the mean for the control cell lines in each case. Error bars indicate the standard deviation. Heavy strand tRNAPhe and tRNALeu expression is reduced relative to light strand tRNA Gln in m.547A>T fibroblasts (A, p<0.001) and cybrids (C, p<0.001 for tRNA Phe(F), Val (V) and Leu (L)). Experiments were repeated three times with equivalent results. Labelling for 5S rRNA was used to confirm equal loading. Heavy chain transcripts RNR1 (B) and CO1 (D) were measured by quantitative RT-PCR and were reduced in m.547A>T cybrids relative to the light strand transcript ND6. Each point represents the mean of several independent cybrid cell lines derived from a single donor.</p

Mitochondrial function is impaired in m.547A>T fibroblasts and cybrids.

<p>Oxygen consumption rate (OCR) was measured to assess mitochondrial function in fibroblasts (A, C) and cybrids (B, D), normalised for cell number. Representative comparison of fibroblasts (A) and cybrids (B) from control individuals (red) with fibroblasts or cybrids from patients with the m.547A>T substitution (blue) showing a substantial change in respiratory profile. There was a significant decrease in baseline oxygen consumption, and in maximal oxygen consumption following addition of FCCP in both fibroblasts (C) and cybrids (D). Asterisks *p < 0.05, **p < 0.005, and ***p < 0.001 for control versus patient groups, represented as the mean ± SD of separate experiments performed in triplicate with four patient and four control cell lines.</p

mt.616T>C cybrids have a defect in respiration.

<p>(A) Two pedigrees showing potential maternal inheritance of renal disease. Individuals with kidney disease are represented by filled shapes as in <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1006620#pgen.1006620.g001" target="_blank">Fig 1</a>. Family 8 from ref 13 forms part of pedigree II, and is indicated by the dotted box. Pedigree III is Family 6 from ref 13. Individuals from whom DNA was sequenced in the current study are marked with asterisks. All affected individuals who were sequenced were found to have homoplasmic levels of the m.616T>C substitution. The mitochondrial haplotype is T1a1. (B) Measurement of oxygen consumption in patient-derived and control cybrids showing a reduction in basal (before addition of oligomycin) and maximal respiration (after addition of FCCP) in patient-derived cybrids. (C) Expression levels of tRNAs quantified by Northern blot of three control and patient-derived cybrids show reduced mitochondrial tRNAPhe levels relative to the light strand encoded tRNAGln in mt.616T>C cells.(p = 0.006) The tRNA levels for valine and leucine were unaffected. (D) Conservation of mt tRNA Phe within vertebrates. The anticodon (GAA) is highlighted in bold, the nucleotides forming the last pair of the anticodon stem are underlined. Sequences were aligned with clustal omega and manually adjusted. The stem (s) and loop (l) secondary structure of the tRNA Phe of humans is indicated at the bottom.</p