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Mccallum, Monica – Imaging the Microbial Community of the Marine

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Mccallum, Monica – Imaging the Microbial Community of the Marine Microbial Diversity Course Marine Biological Laboratory July 8 to August 22, 2018 Imaging the Microbial Community of the Marine Sponge Clathria prolifera Monica E. McCallum, Ph.D. Department of Chemistry and Chemical Biology Harvard University BACKGROUND Marine sponges are prolific producers of biologically active compounds and are particularly valued as sources of novel antibiotics and chemotherapeutics. The sponges themselves provide housing and nutrients for a complex microbial community that accounts for approximately 40% of any sponge’s mass and likely produces these complex bioactive natural products.1 However, the cultivation of these microbial symbionts, which would facilitate the study of their biosynthetic capabilities, has proven to be immensely challenging. Understanding the niche of microbial species within the sponge microbiome may help facilitate culturing of these organisms away from their sponge host for further study. In the early 2000s, three successive MBL Microbial Diversity students attempted to interrogate the microbial populations of three different local sponge species.2 The first was conducted by Dovi Kelman in 2001 on the local sponge Suberites ficus. Two years later, Gil Zeidner profiled the microbial community of the local sponge Holichondria sp. and was able to detect archaea using FISH microscopy with the ARCH915 probe.2b Kou-San Ju constructed a small 16s rDNA library of Clathria prolifera using universal Eubacterial primers 9F and 1492.2c Subsequent cloning into E. coli and sequencing led to the identification of 42 unique species across 14 types of bacteria, but no mention was made of any archaea present. Clathria prolifera, which is commonly known as the Red Beard Sponge, is available from the MBL MRC and has been studied extensively as a model organism for instruction in biology and environmental science, but its microbiome has been minimally surveyed.3 The microbiomes of other marine sponges have been extensively catalogued by the Sponge Micrbiome Project.4 However, little is known of the archaeal symbionts of marine sponges, though sequences corresponding to ammonia oxidizing archaea are frequently reported in sponge metagenomic studies. DeLong and coworkers described the first symbiotic association of a sponge (Axinella mexicana) and archaeon (Cenarchaeum symbiosum) in 1996.5 A decade later, DeLong and coworkers reported the first genomic analysis of C. symbiosum, but to date that organism remains uncultivated.6 The first marine crenarchaeon to be isolated in pure culture was a free- living autotrophic ammonia-oxidizer,7 but the subsequent cultivation of additional ammonia oxidizing archaea from marine environments has been limited. Sponges are important to nutrient and nitrogen cycling in the ocean, but the bacteria and archaea within these sponges may be responsible for the majority of nitrogen flux. Ammonia oxidizing archaea (AOAs) and bacteria (AOBs) have been found in a diverse array of sponges throughout the Earth’s oceans via 16S sequencing and via PCR amplification of the ammonia monooxygenase subunit A (amoA).8,9,10 Cultivation of an AOA, or any archaeon, from a sponge has yet to be reported. This miniproject aimed to use a variety of microscopy techniques to determine where different microbes reside within the sponge host C. prolifera and to attempt to enrich ammonia oxidizing archaea from C. prolifera. RESULTS AND DISCUSSION The marine sponge C. prolifera is a Demosponge with a skeleton made of spongin spicules that grows in shallow fast-flowing water along the coast of Falmouth, MA. The branching structure of C. prolifera provided easily accessible portions of sponge tissue for repeated sampling with minimal trauma to the sponge (Fig. 1a). The sponge tissue was homogenized via bead beating (Fig. 1b-c, d-e) and used to inoculate enrichment cultures containing minimal medium tailored to cultivate chemolithoautotrophic ammonia oxidizing archaea and bacteria. Growth of ammonia oxidizers was monitored using the colorimetric Griess test to observe the nitrite produced by this metabolism. After two weeks, none of the enrichment cultures had ever tested positive for nitrite and only a single tube of this enrichment showed visible growth (Fig. 1f). Figure 1. (a) the marine sponge Clathria prolifera (b) excised live sponge tissue (c) homogenized live sponge tissue (d) excised dead sponge tissue (e) homogenized dead sponge tissue (f) biofilm growing on enrichment culture after 14 days. The sample of C. prolifera contained two distinct regions of tissue: bright orange, live sponge tissue (Fig. 1b) and brown, dead tissue (Fig. 1d). Under differential interference contrast (DIC) light microscopy, these two tissues had distinct morphological features (Fig. 2). The live tissue consisted primarily of round sponge tissue cells interspersed with the spongin spicules that provide structural support in the sponge. The dead tissue contained few intact sponge tissue cells and was dominated by large, fast-moving microbes with spiral morphology and a variety of amoeba and ciliates. Figure 2. DIC images of live sponge tissue (left) and dead sponge tissue (right) at 40x magnification. After observing the sponge tissues under light microscopy, a series of observations were made using fluorescence microscopy. From this, it was determined that the sponge tissue and its microbial inhabitants exhibit bright autofluorescence under every filter cube set available on the Zeiss microscope (Fig. 3). Both the live sponge tissue and the dead sponge tissue exhibited autofluorescence, though it appeared to be qualitatively less in the dead sponge tissue. Figure 3. Autofluorescence of (a) live sponge tissue homogenate (b) dead sponge tissue homogenate. Labels in top left indicate filter cube used to acquire the image – no fluorescent probes were added. In hopes of overcoming the inherent autofluorescence of the sponge tissue to image its microbial symbionts, the samples were incubated with a series of fluorescent probes. Figure 4 shows the staining of lectins (top left) present in the biofilm from the enrichment culture that was inoculated with homogenized live sponge tissue. The aggregates of enriched microbes seen under brightfield light microscopy do not exhibit autofluorescence (Fig. 4, bottom left) but do stain with ConA-rhodamine. Microbes that are not aggregated do not stain with ConA-rhodamine. Conversely, attempts to employ mono fluorescence in situ hybridization (FISH) with EUB-Alexa488 and ARCH915-Cy3 to stain bacteria and archaea respectively and overcome the autofluorescence of the sponge failed (Fig. 4, right). Figure 4. (a) lectin staining (top) of the culture containing the biofilm and control for autofluorescence (bottom); (b) attempted monoFISH with EUB-Alexa488 and ARCH915-Cy3 on fixed live sponge tissue (top) and fixed dead sponge tissue (bottom). Labels in top left indicate filter cube and fluorescent probe used to acquire the image. Having failed to overcome the sponge autofluorescence with mono-FISH, microbial identification through passive clarity technique (MiPACT) was attempted.14 Samples of sponge tissue were embedded in resin, cleared with SDS, and cut into 1 mm3 pieces prior to incubation with probes for hybridization chain reaction FISH (HCR-FISH), which amplifies the fluorescence signal by an order of magnitude as compared to mono-FISH. An additional benefit of this technique is that embedding the tissue in resin and imaging using confocal microscopy allows for 3D reconstructions of the environment inside of the sponge. Samples of sponge tissue were prepared for MiPACT with no HCR-FISH probe, EUB B1 probe, or NON B1 probe. Sections of the sponge tissue were imaged in 10 x 80 x 80 um cubes. Without a HCR-FISH probe, the DAPI present in the mounting medium stained the nuclei of the sponge cells, which were visible as blue spheroids in Figure 5a. The autofluorescence of the sponge was still visible under confocal microscopy, particularly around the spicules (top right of Fig. 5a), but it appeared to be greatly diminished as compared to the standard fluorescence microscopy carried out earlier. For the sample containing EUB B1 probe, there is a strong signal from the Alexa-488 fluorophore that may be colocalized with bacterial symbionts (small spheroids and rods, Fig. 5b). The large green patches present in Figure 5b may correspond to non-specific probe binding or to thick biofilms coating the interior of the pores in the sponge tissue. However, the sample with the NON B1 probe, which is a nonsense rearrangement of the bases in the EUB B1 probe with an Alexa-488 fluorophore, does not show this pattern and looks similar to the tissue sample without HCR-probe treatment. With optimization, this technique could be used to visualize the 3D distribution of microbial populations on and within the sponge tissue, perhaps even intracellularly. Figure 5. Stills from a 10 um z-stack of (a) DAPI-only stain of MiPACT–prepared live sponge tissue (b) DAPI, EUB B1, and Con-A stained MiPACT-prepared live sponge tissue In an attempt to determine what microbes were present on the sponge tissue, samples of live and dead sponge tissue were homogenized and their metagenomic DNA was extracted. 16S rDNA was amplified using archaeal specific primers in hopes of obtaining sequences corresponding to ammonia oxidizing archaea. The crude amplification reactions were ligated into a pGEM-T vector system and clones containing inserts were identified via blue/white selection. These clones were cultured, miniprepped,
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