Microbial Ecology, Marine Microbiology, Microbial Diversity

Microbial biogeochemistry in Hawaiian lava tubes

Metabolically active microbial communities are detected in ever more extreme environments, such as subsurface basalt aquifers, granite batholiths and the oceanic crust. Understanding how these communities thrive under what are generally highly oligotrophic conditions is a new frontier. New work in this field is being enabled by both novel techniques and new approaches with extant technology. By determining how single cells and communities interact at the molecular level with each other, with their environment, and with potential sources of energy, we and our collaborators aim to bring new insights into the environmental control of microbial diversity and physiology, and help interpret the fossil record and exobiology.

We aim to identify and understand processes through which microorganisms derive energy by interacting with metals and minerals. For example, chemolithoautotrophy is important where labile carbon may be in short supply, e.g., deep-sea hydrothermal vents, terrestrial geothermal features, and high altitude, xeric settings. In this respect, volcanic materials are among the most ubiquitous rock types on the Earth's surface, yet how microbes interact with a volcano per se, particularly on fresh or moderately weathered lava, has been largely overlooked. Hawai'i Volcanoes National Park (HVNP) is an excellent terrestrial site in which to investigate microbial community structure under highly nutrient limited conditions. Along with fumaroles, gases and rain, the scene is reminiscent of conditions that prevailed on much of early Earth. We hypothesize that members of the microbial community here derive energy by oxidizing elements in lava, such as Fe and Mn, and that they require nutrients from the dissolution of primary minerals, e.g., P, Mo and V. The mechanisms they use to colonize and alter host rocks may be specific to terrestrial chemolithoautotrophs, or may be cosmopolitan.

Lava caves in Kilauea are an attractive habitat type in which to investigate microbial interactions with the environment. The rock substrates are very young, UV-exposure variable, and water availability may be low. How these factors might affect hypogean (cave) microbial communities in terms of phylogeny, physiology, gene expression, growth rates, nutrient cycling and lithoautotrophic alteration of basalt substrates, are some of the questions we propose to investigate here. By examining natural microbial communities, as well as the colonization of substrates in situ and in the laboratory, we anticipate discovering novel microbes (and new biogeochemical functions for previously known microbes) through cell-specific and oligotrophic culturing techniques.

Collaborators

  • Alexis Templeton, University of Colorado
  • Jamie Foster, University of Florida, Kennedy Space Center
  • Hubert Staudigel, Scripps Institution of Oceanography, University of California, San Diego
  • Stephan Kempe Technical University of Darmstadt, Darmstadt, Germany

Host-microbe associations in Hawaiian marine invertebrates

Many microorganisms form associations with marine eukaryotes (Polz et al. 1999; Webster et al., 2001; Gillan & Dubilier, 2002; Hentschel et al., 2002; Rohwer et al., 2002; Fieseler et al., 2004). Such associations may provide nutrients or dietary co-factors to the host, or perhaps molecules that protect the host from 'infection' by other microbes, or ingestion by other eukaryotes (Holmstrom & Kjelleberg, 1994; Donachie & Zdanowski, 1998; Mearns-Spragg et al., 1998). Although Hawaii's marine eukaryotes have been extensively catalogued, with new species still being discovered, most of the work published on associations between such eukaryotes and microbes has focused on Vibrio fischerii in the Hawaiian Bobtail squid, Euprymna scolopes (e.g., Montgomery & McFall-Ngai, 1994).

With thousands of endemic and native marine eukaryotes throughout the Hawaiian Archipelago, however, there is significant potential that new microorganisms (Archaea, Bacteria and Eucarya) will be discovered (sensu Staley, 1997). It is equally likely that such microorganisms will provide novel secondary metabolites of either clinical or industrial importance. Through this project we aim to describe microbial diversity in selected Hawaiian marine invertebrates, isolate and describe novel microbes, determine what may be the role of commensal or symbiotic microbes in the host, and also screen cultivated microbes for secondary metabolites.

Literature Cited

  • Donachie SP & MK Zdanowski (1998) Potential digestive function of bacteria in krill, Euphausia superba stomach. Aquatic Microbial Ecology 14:129-136
  • Fieseler L, M Horn, M Wagner & U Hentschel (2004) Discovery of the novel Candidate phylum “Poribacteria” in marine sponges. Applied & Environmental Microbiology 70:3724-3732
  • Gillan DC & N Dubilier (2004) Novel Epibiotic Thiothrix bacterium on a marine amphipod. Applied & Environmental Microbiology 70:3772-3775
  • Hentschel U, J Hopke, M Horn, AB Friedrich, M Wagner, J Hacker & BS Moore ( 2002) Molecular evidence for a uniform microbial community in sponges from different oceans. Applied & Environmental Microbiology 68:4431-4440
  • Holmstrom C & S Kjelleberg (1994) The effect of external biological factors on settlement of marine invertebrates and new antifouling technologies. Biofouling 8:147–160
  • Mearns-Spragg A, M Bregu, KG Boyd & JG Burgess (1998) Cross-species induction and enhancement of antimicrobial activity produced by epibiotic bacteria from marine algae and invertebrates, after exposure to terrestrial bacteria. Letters in Applied Microbiology 27:142–146
  • Montgomery MK & MJ McFall-Ngai MJ (1994) Bacterial symbionts induce host organ morphogenesis during early postembryonic development of the squid Eupyrmna scolopes. Development 120:1719–1729
  • Polz MF, C Harbison & CM Cavanaugh (1999) Diversity and heterogeneity of epibiotic bacterial communities on the marine nematode Eubostrichus dianae. Applied & Environmental Microbiology 65:4271-4275
  • Webster NS, KJ Wilson, LL Blackall & RT Hill (2001) Phylogenetic diversity of bacteria associated with the marine sponge Rhopaloeides odorabile. Applied & Environmental Microbiology 67:434-444
  • Rohwer F, V Seguritan, F Azam3 & N Knowlton (2002) Diversity and distribution of coral-associated bacteria. Marine Ecology Progress Series 243:1-10

Anti-infective and cytotoxic secondary metabolites in Fungi and yeasts from Hawaiian marine environments

Hawaii's marine mycoflora is phylogenetically diverse and in some cases unique to the Hawaiian archipelago (Donachie et al., 2004). Since much of this flora is unlikely to have had little if any contact with clinically important bacterial or fungal pathogens, we predict that secondary metabolites expressed by Hawaii's marine mycoflora may be effective against emerging microbial threats, and any or all of a range of human cancer cells. Just a handful of terrestrial microorganisms provide most currently used antibiotics. Using only a narrow range of antibiotics, however, risks the development of resistance developing and spreading among pathogens. For example, vancomycin is widely considered a 'last resort' treatment when other drugs have proven ineffective, but resistance to this potent antibiotic among enterococci is a growing threat. The threat is enhanced when one considers the likelihood of transfer of resistance from vancomycin resistant enterococci to other bacteria.

To counter the growing threat posed by antibiotic-resistant bacteria, Fungi and yeasts, we must expand the diversity of antimicrobial agents available to medical professionals. Material from under-represented taxa and unexplored sites or niches is ideal starting material (Colwell, 1997, 2000). In this respect, the collection of marine-derived Fungi and yeasts we have established is a valuable resource. Discovery work in the field of bio-active secondary metabolites has tended to focus on non-microbial sources, such as marine invertebrates, but because the target molecule is usually present in extremely low concentrations these sources rarely meet the demand for raw material (Jensen & Fenical, 2000, 2002). Marine microorganisms can meet the material demand because large quantities are generally easy to produce. In this project we are isolating Fungi and yeasts from diverse marine habitats around Hawai'i, and screening cultivated strains for antibiotic and cytotoxic activities. As of October 2006, a total of 689 isolates have been cultivated, ~90% of which have been sequenced and submitted to Genbank with accession numbers EF060395-EF060975 (http://www.ncbi.nlm.nih.gov/).

Collaborators

  • Prof. Thomas K. Hemscheidt, Department of Chemistry, University of Hawai'i (Manoa)
  • Prof. Jack Fell, Rosenstiel School of Marine and Atmospheric Science, University of Miami

Literature Cited

  • Colwell RR (1997) Microbial diversity: the importance of exploration and conservation. J. Ind Microbiol. Biotechnol. 18:302-307
  • Colwell RR (2000) Biocomplexity and the oceans. Sea Technology 41:22-23
  • Donachie SP, S Hou, K-S Lee, CW Riley, A Pikina, C Belisle, S Kempe, TS Gregory A Bossuyt, J Boerema, J Liu, TA Freitas, A Malahoff & M Alam (2004a) The Hawaiian Archipelago: A Microbial Diversity Hotspot. Microbial Ecology 48:509-520 [pdf]
  • Jensen PR & W Fenical (2000) Marine microorganisms and drug discovery: Current status and future potential. In Fusetani N (ed) Drugs from the sea. Basel, Karger, pp. 6-29
  • Jensen PR & W Fenical (2002) Secondary metabolites from marine fungi. In: Hyde KD (ed) Fungi in Marine Environments. Fungal Diversity Research Series 7:293-315