Deep-sea corals have complex microbial assemblages, just like shallow corals

This is the second in a series of five referenced articles about shared characteristics between deep and shallow water corals

Special guest post by Christina A. Kellogg

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Just as humans have beneficial bacteria living on our skin and in our intestines, corals have symbiotic microbes in their mucus, tissues, and skeletons. Unfortunately, there are also disease-causing microbes that can infect corals. These coral-associated microbes include all three of the major domains of life: Bacteria, Archaea, and Eukarya (fungi, and in shallow-water corals, algae) and also viruses (Rosenberg et al. 2007). Identifying and characterizing these coral-associated microbes is a relatively new field, in which most of the key information has been generated within the past decade and mainly from shallow-water species. So who are these coral-associated microbes and what do they do?


Algae: The best known microbial associates of shallow-water corals are zooxanthellae–the symbiotic dinoflagellates that photosynthesize and provide energy to the coral animal in the form of carbon compounds. Zooxanthellae were originally considered a single species, but molecular techniques have revealed that there are multiple genetically diverse groups that have different distributions, host-specificity, and stress tolerances (Reviewed in Baker 2003). It is generally believed that this symbiosis increases the coral’s rate of calcification. However, there are azooxanthellate shallow-water corals (Marshall 1996) and deep-water corals (Bell & Smith 1999) with comparable calcification rates, which suggest that development of coral reefs may not be as tightly linked to light-enhanced calcification as previously thought. Moreover, it raises the question of how azooxanthellate corals (both shallow and deep) compensate without the dinoflagellates. Shallow-water corals may also contain endolithic algae. These algae bore into the coral skeleton, and can be seen as color bands in sectioned corals (see Fig 2). When a coral bleaches (i.e., loses its zooxanthellae due to thermal stress or disease), the endolithic algae can provide some nutrients to support the coral until it can reestablish its zooxanthellae (Fine & Loya 2002).

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Bacteria: Multiple studies have shown that corals host complex and diverse bacterial communities that are distinct from those in the water column: Examples of shallow-water studies include Ritchie & Smith 1995, Rohwer et al. 2001, Frias-Lopez et al. 2002, Bourne & Munn 2005, and there are two recent deep-water studies, Penn et al. 2006 and Yakimov et al. 2006. It has also become clear that different species of corals have different bacterial communities (Rohwer et al. 2002) and that there is evidence of specific bacteria-coral interactions; where a particular bacterial species (represented by a unique 16S rRNA gene sequence) or group of species have been repeatedly found in association with multiple individuals within a coral species (Shallow-water: Rohwer et al. 2001, Bourne & Munn 2005, Webster & Bourne 2007; Deep-water: Kellogg 2007). The presence of coral species-specific bacteria makes it clear that these interactions are not random or passive.

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Our understanding of the specific roles filled by coral-associated bacteria is just beginning, but it has been speculated that coral-associated bacteria benefit the coral by fixing nitrogen, breaking down waste products, and (in shallow-water corals) cycling basic nutrients back to the zooxanthellae (Shashar et al. 1994, Rohwer et al. 2001, Lesser et al. 2004). Bacteria may also ward off other potentially harmful microbes by producing antibiotics or just by occupying the available space (Dobretsov & Qian 2004, Ritchie 2006). Coral-associated bacterial populations are closely attuned to host metabolism and may change in number or composition in response to a change in coral health (Ducklow & Mitchell 1979, Pantos et al. 2003).

Archaea: Archaea are associated with shallow-water corals, but their functions remain unknown (Kellogg 2004, Wegley et al. 2004). A recent study found archaeal ammonia monooxygenase gene expression associated with five species of corals (Beman et al. 2007). This gene encodes the first step of a pathway that converts ammonia to nitrite or nitrate, so these archaea may be removing host waste products like ammonia and urea. Attempts have been made to detect archaea in deep-sea corals, but have not yet been successful (Yakimov et al. 2006, Kellogg 2007).

Fungi: Fungi are found in both shallow and deep coral species, but it seems that they are pathogens or part of the microbial complex that alters the coral after death (Freiwald et al. 1997, Bentis et al. 2000, Priess et al. 2000, Ravindran et al. 2001).

Scientists are interested in these microbial communities not only because they are integral to coral biology and ecology, but also because their study contributes to our knowledge of microbial diversity and biogeography. Corals are microbial landscapes hosting an amazing diversity of life (Knowlton & Rohwer 2003). While shallow-water corals are characterized by their photosynthetic algal symbionts, bacteria and archaea are beginning to be seen as symbionts in their own right. It remains to be determined whether bacteria and archaea play an even larger role in deep-sea corals to offset the lack of photosynthetic partners.

Web links:

http://coastal.er.usgs.gov/coral-microbes/

(For a printable version of this web site, visit http://pubs.usgs.gov/fs/2005/3039/)

References:
Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annual Review of Ecology, Evolution and Systematics 34:661-689

Bell N, Smith J (1999) Coral growing on North Sea oil rigs. Nature 402:601

Beman JM, Roberts KJ, Wegley L, Rohwer F, Francis CA (2007) Distribution and diversity of archaeal ammonia monooxygenase genes associated with corals. Applied and Environmental Microbiology 73:5642-5647

Bentis CJ, Kaufman L, Golubic S (2000) Endolithic fungi in reef-building corals (Order: Scleractinia) are common, cosmopolitan, and potentially pathogenic. Biological Bulletin 198:254-260

Bourne DG, Munn CB (2005) Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environmental Microbiology 7:1162-1174

Dobretsov S, Qian P-Y (2004) The role of epibiotic bacteria from the surface of the soft coral Dendronephthya sp. in the inhibition of larval settlement. Journal of Experimental Marine Biology and Ecology 299:35-50

Ducklow HW, Mitchell R (1979) Bacterial populations and adaptations in the mucus layers on living corals. Limnology and Oceanography 24:715-725

Fine M, Loya Y (2002) Endolithic algae: an alternative source of photoassimilates during coral bleaching. Proceedings of the Royal Society of London Series B-Biological Sciences 269:1205-1210

Freiwald A, Reitner J, Krutschinna J (1997) Microbial alteration of the deep-water coral Lophelia pertusa: Early postmortem processes. Facies 36:223-226

Frias-Lopez J, Zerkle AL, Bonheyo GT, Fouke BW (2002) Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces. Applied and Environmental Microbiology 68:2214-2228

Kellogg CA (2004) Tropical Archaea: diversity associated with the surface microlayer of corals. Marine Ecology Progress Series 273:81-88

Kellogg CA (2007) Microbial diversity associated with Lophelia pertusa in the Gulf of Mexico Twenty-fourth Gulf of Mexico Information Transfer Meeting. U.S. Depart. of Interior, Minerals Management Service, Gulf of Mexico OCS Region, New Orleans, LA

Knowlton N, Rohwer F (2003) Multispecies microbial mutualisms on coral reefs: the host as a habitat. The American Naturalist 162:S51-S62

Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG (2004) Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305:997-1000

Marshall AT (1996) Calcification in hermatypic and ahermatypic corals. Science 271:637-639

Pantos O, Cooney RP, Le Tissier MDA, Barer MR, O’Donnell AG, Bythell JC (2003) The bacterial ecology of a plague-like disease affecting the Caribbean coral Montastrea annularis. Environmental Microbiology 5:370-382

Penn K, Wu D, Eisen JA, Ward N (2006) Characterization of bacterial communities associated with deep-sea corals on Gulf of Alaska seamounts. Applied and Environmental Microbiology 72:1680-1683

Priess K, Le Campion-Alsumard T, Golubic S, Gadel F, Thomassin BA (2000) Fungi in corals: black bands and density-banding of Porites lutea and P. lobata skeleton. Marine Biology 136:19-27

Ravindran J, Raghukumar C, Raghukumar S (2001) Fungi in Porites lutea: association with healthy and diseased corals. Diseases of Aquatic Organisms 47:219-228

Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Marine Ecology Progress Series 322:1-14

Ritchie KB, Smith GW (1995) Preferential carbon utilization by surface bacterial communities from water mass, normal and white-band diseased Acropora cervicornis. Molecular Marine Biology and Biotechnology 4:345-352

Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N (2001) Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 20:85-91

Rosenberg E, Kellogg CA, Rohwer F (2007) Coral microbiology. Oceanography 20:114-122

Shashar N, Cohen Y, Loya Y, Sar N (1994) Nitrogen fixation (acetylene reduction) in stony corals: evidence for coral-bacteria interactions. Marine Ecology Progress Series 111:259-264

Webster NS, Bourne DG (2007) Bacterial community structure associated with the Antarctic soft coral, Alcyonium antarcticum. FEMS Microbiology Ecology 59:81-94

Wegley L, Yu Y, Breitbart M, Casas V, Kline DI, Rohwer F (2004) Coral-associated Archaea. Marine Ecology Progress Series 273:89-96

Yakimov MM, Cappello S, Crisafi E, Trusi A, Savini A, Corselli C, Scarfi S, Giuliano L (2006) Phylogenetic survey of metabolically active microbial communities associated with the deep-sea coral Lophelia pertusa from the Apulian plateau, Central Mediterranean Sea. Deep Sea Research 53:62-75

Peter Etnoyer (406 Posts)

PhD candidate at Texas A&M University- Corpus Christi and doctoral fellow Harte Research Institute for Gulf of Mexico Studies.





3 comments on “Deep-sea corals have complex microbial assemblages, just like shallow corals
  1. Yay! Microorganisms!!

    Chris, a nice post. I’m looking forward to seeing you in July at ICRS – it should be a fun meeting (and our first coral outing!).

    Thouhts on why you might not be finding Archaea yet in deep-water corals? Curious.

  2. “Thoughts on why you might not be finding Archaea yet in in deep-water corals?”

    I think it has to be a methodological shortcoming–either there is an inhibition of the PCR, or the species of Archaea are just different enough that the ‘standard’ archaeal primer sets aren’t picking them up. As abundant as Archaea are in deep-sea sediments and the water column, and knowing they are present in shallow-water corals, I can’t believe they aren’t there…

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