Microbial Ecology of Four Pacific Coral Atolls

In this study, the coral reef microbial communities associated with four neighbouring coral atolls in the Northern Line Islands (central Pacific) were compared measuring:

• The abundance of Bacteria, Archaea, Protists and Virus-like particles (VLPs) using direct counts on water samples.
  
• Abundances of culturable Vibrio spp. by counting colony forming units (cfu).
• The taxonomical and metabolic potential of the microbial and viral communities using metagenomic analyses.
• The water chemistry (total dissolved inorganic nitrogen compounds, phosphate, and DOC) and the "nutritional quality" of the water (Respiration rate).
• The coral health (percent cover and disease prevalence), the percent cover of other benthic organisms and the fish biomass.

The most northern atoll, Kingman, is a small, pristine and uninhabited atoll with microbial and water chemistry characteristic of an open ocean oligotrophic ecosystem. In contrast, Kiritimati, which lies most southerly in the chain, is a large and populated atoll, with microbial and water chemistry characteristic of a near-shore environment. The middle atolls, Palmyra and Tabuaeran, have intermediate sizes and water characteristics if compared to Kingman and Kiritimati.

The results obtained by the authors, showed a steady increase in total dissolved inorganic nitrogen and phosphate moving south from Kingman to Kiritimati. In contrast, dissolved organic carbon (DOC) concentrations were highest on Palmyra and Tabuaeran and lowest on Kiritimati. In parallel with these differences in water chemistry, microbes, VLPs and protists densities increased steadily across the four atolls. Microbial communities were increasingly autotrophic moving from Kingman to Palmyra to Tabuaeran, but the proportion of autotrophs sharply declined on Kiritimati, where a sharp increase in heterotrophic Bacteria and Archaea and in potential pathogens (e.g. Vibrio spp.) was observed. The most common autotrophic bacteria in the oligotrophic waters of Kingman and Palmyra was Prochlorococcus, whereas Synechococcus, which tends to becomes dominant in nutrient rich water, was the most common on Tabuaeran and Kiritimati. In parallel with the microbial analysis, the analysis of the phage hosts showed the phage known to infect cyanobacteria increased progressively from Kingman to Palmyra and Tabuaeran, and then at Kiritimati the phage known to infect heterotrophic microbes became dominant. In addition, fish biomass and coral coverage sharply declined from Kingman to Kiritimati, while coral disease incidence and algal cover were lowest on Kingman and highest on Kiritimati.

The authors formulated two competing but not mutually exclusive hypotheses to explain the observed microbial and macrobiota differences across the four atolls which could reflect regional variation in either oceanographic/hydrographic conditions or in the human impact on the ecosystem. Moving south from Kingman in fact, the atolls became progressively larger with a greater potential to induce upwelling, higher land run-off, larger lagoons, and to support larger seabird populations. All of these factors together with the increasing levels of human disturbance (sewage, agricolture and fishing) and with varying amounts of temperature stress associated with anthropogenic global warming, can easily alter the characteristics of seawater, increasing noticeably the amount of nutrients in the water column.

The main hypothesis is that the increase of nutrients (mainly nitrogen and phosphate) from upwelling and land runoff, on the progressively larger atolls, combined with a loss of herbivory (fishing), can stimulates the growth of benthic macroalgae and phytoplankton. In turn, this algae produces labile DOC (that is an available carbon source) which supports more heterotrophic bacterial growth, explaining thus, the increase in total microbes number, the shift in the microbial community from autotrophic to eterotrophic and the increase in algal cover observed on Kiritimati atoll.

The excess of DOC may be also a primary driver of coral-microbial interactions. As a matter of fact, it can increase microbial growth on the corals, which in turn can cause hypoxia and presumably the coral mortality. Moreover, the observed ten-fold increase in potential pathogenic bacteria on Kiritimati, could be caused either by an increased input of human and animal pathogens from land or by the increase in algal-derived DOC (either by stimulating the growth of pathogens or by promoting algal-associated pathogenic communities). Whatever the source is, this increase in pathogenic bacteria, may easily explaine the increased coral mortality observed on Kiritimati.

Another options proposed by the authors, it that a recent bleaching event killed the corals, and then algae could have colonized the area. In this case the microbial mechanisms discussed above could help prevent recolonization by corals. The most plausible hypothesis, however, is that overfishing removes both predatory and herbivorous fish. Loss of the herbivorous fish results in higher algal growth, which leads in turn, to an increase in DOC which can supports more heterotrophic and pathogenic microbes, probably the main responsible of coral death (either as primary causes or as opportunistic pathogens that kill the weakened bleached corals). Whichever the correct hypotesis is, it's clear that marine microbes play a key role in the complex feedback mechanism between humans, fish, algae and corals that clearly requires further investigations.

Reference:

Dinsdale E.A., Pantos O., Smriga S., Edwards R.A., Angly F., Wegley L., Hatay M., Hall D., Brown E., Haynes M., Krause L., Sala E., Sandin S.A., Thurber R.V., Willis B.L., Azam F., Knowlton N., Rohwer F., (2008). Microbial ecology of four coral atolls in the Northern Line Islands. PLoS One 3:e1584.