Marine bacteria use swimming behavior to colonize coral hosts

Corals develop important beneficial, and sometimes detrimental, relationships with a range of microorganisms, including algae and diverse populations of bacteria and archaea, but little is currently known about the microbial behaviors involved in the establishment and maintenance of coral-microbe interactions. We applied a suite of approaches, including microfluidic experiments and genomic analysis, to investigate the extent to which natural communities of coral associated microbes use deliberate swimming behavior to colonize a coral host.

HFSP Young Investigator Grant holders Justin Seymour and Roman Stocker and colleagues
authored on Tue, 25 August 2015

Corals are sessile, benthic (bottom-dwelling) marine animals that generate a hard exoskeleton made up of calcium carbonate. They are a dominant ecological feature in tropical regions of the ocean where they form the framework for immense living ecosystems, known as coral reefs, which are the largest living structures on earth. Coral reefs host levels of biodiversity that parallel tropical rainforests and they sustain the productivity and biodiversity of tropical fish species, supporting important fisheries worldwide. This, combined with their popularity as tourism locations and their role in protecting coastal environments from wave energy, generates an estimated economic value of > $375 billion USD per year.

Photo by Jessica Tout.

The coral animals that compose coral reefs do not live in isolation, rather they form important ecological relationships with a variety of microorganisms. The microorganisms living in association with corals play a number of ecological roles, ranging from symbiotic relationships that provide the coral host with essential nutrients and resources for growth, to pathogenic interactions that have been implicated in several coral diseases.  It is becoming clear that the balance of these coral-microbe interactions has a fundamental influence on coral health, and in some instances may be involved in the current world-wide decline of coral reefs. While molecular biological approaches have taught us much about the diversity and composition of coral associated microbial assemblages during the last decade, we still know very little about the behavioral and ecological processes involved in coral-microbe relationships.

Our aim was to determine whether natural populations of coral reef bacteria are able to use deliberate behaviors to directly establish and maintain associations with coral hosts. We were particularly interested in a behavior called chemotaxis, which is the ability of microorganisms to sense chemical gradients and subsequently migrate towards regions enriched in favorable compounds.  Previous studies using isolated laboratory strains of bacteria have indicated that chemotaxis may play a role in the onset of some coral diseases, but little is known about the capacity of natural communities of bacteria to use chemotaxis to migrate towards the chemicals released by corals.

We performed a series of experiments at Heron Island, which is located within the Great Barrier Reef, Australia. Using a combination of laboratory experiments and in situ studies conducted on the reef itself, we examined whether natural coral reef bacteria exhibit chemotactic behavior towards a suite of chemicals known to be released by corals. The in situ experiments involved the use of a microfluidic-based platform, called the In Situ Chemotaxis Assay. This device consists of an array of small chambers, which are filled with different chemical attractants that diffuse from the chambers into the external seawater and effectively act as ‘bait’ for bacteria in the seawater. When bacteria are attracted to a specific chemical they migrate into the chambers and we subsequently count the numbers of bacteria responding to a given chemical and identify them using DNA sequencing approaches.

These experiments revealed that coral reef bacteria demonstrate extremely high levels of chemotaxis to a wide range of chemicals produced by corals, indicating that chemotaxis is likely to play an important role in the development of microscale associations between corals and bacteria. Notably, we found that bacterial communities occurring immediately adjacent to corals displayed a much higher propensity for chemotactic behavior than bacterial populations living in nearby open water. This observation was supported by an additional survey of the genomic content of coral-associated and non-coral associated bacterial communities, which demonstrated a substantially higher proportion of genes involved in chemotaxis and swimming motility among the coral associated bacteria. These patterns imply that relative to other populations of planktonic bacteria, chemotactic behavior has particular ecological importance for coral-associated microbial assemblages.

We also found that different bacterial populations exhibited preferences for different chemicals, providing a mechanism for microscale partitioning and organization of microbial assemblages associated with coral surfaces. Among the bacteria responding to some chemicals were putative pathogens, indicating that these behavioral responses may also play a role in the onset of coral disease.

Taken together the results of our study confirm that natural communities of marine microorganisms have the capacity to employ directed swimming behaviors to colonize or maintain spatial associations with corals. This provides a new ecological mechanism involved in the essential coral-microbe relationship and provides further evidence for the importance of microbial behavior within ocean ecology.

Reference

Chemotaxis by Natural Populations of Coral Reef Bacteria. Tout JA, Jeffries T, Petrou K, Tyson G, Webster N, Garren M, Stocker R, Ralph P, Seymour JR (2015) The ISME Journal 9(8):1764-1777

Pubmed link