The New Wave of Marine Biology

The frontiers of science are by definition continually shifting. Areas once considered at the forefront of biology may be considered mainstream only a few years later. As HFSP has the support of frontier science at the core of its mission, it must be open to emerging fields. In HFSP’s programs we are seeing increasing interest from scientists studying marine organisms. What are the opportunities for the discovery of new fundamental biological processes in this vast area? Here, Gabriele Procaccini, Maurizio Ribera d'Alcala' and Roberto Di Lauro discuss recent trends and future challenges.

  Gabriele Procaccini and Maurizio Ribera d'Alcala' are group leaders and Roberto Di Lauro is the  President of the Stazione Zoologica Anton Dohrn in Napoli (Italy), a leading institution in the fields of marine biology and ecology. G. Procaccini is particularly interested in the evolutionary ecology of marine organisms, with a special focus on seagrasses, while M. Ribera d'Alcala's  research is focused on plankton (ecology and evolution) and their mutual interactions with abiotic forcing. Roberto Di Lauro is a developmental biologist interested in organogenesis and related diseases.

The oceans occupy 75% of the surface of our planet and comprise over 95% of the volume of the biosphere. Marine organisms, besides being a fundamental resource for studies of biology, genetics and contributing to scientific knowledge in general, fulfil fundamental roles in climate regulation and global biogeochemical cycles. The physics, chemistry, and biology of the oceans are key elements in the functioning of the Earth System. Indeed, life originated in the sea and evolved there into a diverse range of organismal groups before representatives of some of these groups colonised the land. It is notable that marine life is extremely diverse, with many biological phenomena, compounds and lineages that are uniquely found in the sea.

The present loss of biodiversity, catalyzed by just one species, Homo sapiens, is a major concern because of the poorly understood impact of reduced biodiversity on the functioning of the Earth System. Understanding the rules of biodiversity will not in itself reverse the trend but will allow knowledge-based strategies to mitigate it, while providing new insights on the fundamental question of how life evolved on Earth.

Marine biodiversity is not as well understood as its terrestrial counterpart. Unicellular organisms have an extraordinary variety of sizes, shapes and coverings, but we still cannot interpret their function and adaptive value (Fig. 1). Moreover, adaptation to the marine environment has led to convergent morphology in many taxa, making correct taxonomic assignment difficult to assess. Specialized expertise, equipment and services are needed to gather, maintain and study marine organisms. Nonetheless, marine organisms are becoming increasingly important for researchers outside the traditional fields of marine sciences: as biological models to study fundamental biological mechanisms and as sources for innovative products and services with applications across society.

 

Figure 1. Morphological diversity along the diatom lineage. Arrows indicate different modalities of cell junctions between cells joined in chains.

The oceans have long been thought to be more uniform than terrestrial environments, but recent years have seen the discovery of unpredicted levels of diversity, both at the species and at population levels. As an example, a recent estimate suggested that in the deep sea there could be as many as 10 million undescribed species. For bacteria alone, the estimated number of species in the oceans is greater than 500,000 with most being members of the proteobacteria. The past years have seen a breakthrough in marine metagenomics which has paved the way for a new era of molecular marine research. Metagenomics of life in the ocean will yield new insights into ocean biodiversity and the functioning of the marine ecosystem; for the first time it will allow exploration of ecological interrelationships at the gene level. The recent expeditions conducted by the J. Craig Venter Institute looked into the ocean’s microbial diversity, discovering thousands of new species, millions of new genes and thousands of new protein families. In the seminal paper of 2004, the analysis of about 200 litres of surface water from the Sargasso Sea allowed the identification of about 1800 genomic microbial species and 1.2 million unknown genes using an environmental shotgun metagenomic approach (Venter et al., 2004). This study paved the way for further metagenomic approaches, recently reviewed by Gilbert and Dupont (2011), showing how massive sequencing of environmental bacterial samples lead to the discovery of a huge biodiversity and to the unravelling of important components of the pathways of phosphorus, sulphur and nitrogen cycling.

In addition, the establishment of new marine molecular models makes it possible to understand the subtle interactions between plankton and the marine environment as well as the response of more complex organisms to the environment at the neurobiological and behavioural level and will contribute to greatly advance our systemic understanding of marine ecosystems. A recent discovery, which was made possible thanks to the available genome information for the sea urchin Strongylocentrotus purpuratus, highlighted that echinoderms, in contrast to chordates, deploy a microvillar, r-opsin–expressing photoreceptor cell (PRC) type for vision, a feature that has been so far documented only in protostome animals (Ullrich-Luter et al., 2011). Hundreds of thousands of these PRCs are organized in clusters at the base and the tip of the many tube feet, pentaradially distributed on top of the animal skeleton, suggesting that the entire sea urchin body functions as a giant compound eye (Figure 2). This discovery sheds new light on the origin of visual receptors during evolution but it also shows the extent of functional diversity in the marine realm.

Figure 2. Adult specimen of Strongylocentrotus porpuratus with tube feet extended between spines (A), and detail of a tube foot with photoreceptors (B). Panel A is from Ullrich-Luter et al. (2011).

In a further study, a comparative genomic approach revealed that diatoms possess an ornithine-urea cycle, which is involved in the recovery from nitrogen limitation (Allen et al., 2011). The urea cycle is absent in algae and plants and was probably acquired in diatoms through secondary endosymbiosis occurring during the evolutionary history of the group. The presence of both primary and secondary endosymbiosis is another feature of marine organisms which distinguish them from terrestrial ones and which could underlie specific adaptations to the marine environment.

In recent years, the oceans have become more and more attractive for both basic and applied research:

However, an even greater challenge in the ongoing exploration of the sea is to begin to approach very fundamental questions about how the marine environment functions, how organisms interact, what are their adaptive solutions, etc.

Marine science may help in re-balancing the dominant terrestrial-based framework used to approach the functioning and evolution of the marine biota. Our own perception of marine life may be distorted by several factors. For example, we live on a solid substrate, while most marine organisms do not; we are subjected to gravity, while for marine organisms gravity may be almost negligible; we can see for long distances, while this is not possible in the sea; we are tuned to the circadian variability of sunlight, while many marine organisms live hundreds of meters below sea surface where the sun cannot penetrate; we move in a fluid with low resistance (air), while marine organisms deal with a much higher drag; we deal with a rich colour spectrum, while subsurface layers in ocean are deprived of some colours.

Understanding the implications of all the above factors will likely lead to the discovery of unexplored adaptation mechanisms and functionalities that will challenge our current assumptions. They may occur at the level of novel molecular mechanisms, including new metabolic pathways, as hinted by the wealth of unknown genes, but may also occur at higher organizational levels. The interactions in space and time of the unicellular organisms, which are significantly more abundant in the ocean than in terrestrial ecosystems, are far from being understood and even less their ability to condition and “bioengineer” the environment. Little is known about how metazoans interact and, possibly, communicate, and it is absolutely unclear why so many phyla can persist in the marine, compared to the terrestrial environment.

The importance of understanding the complexity of marine ecosystems and their biodiversity and functions is well recognized at the international level. Europe supported the creation of three Networks of Excellence - Marine Genomics Europe, Marbef and Eurocean -  which represented an important step in catalyzing research on different aspects of the marine environment. More recently, the international expedition Tara Oceans is exploring biodiversity along the path of Darwin’s famous expedition around the world, using state of the art metagenomic approaches. The European Strategy Forum on Research Infrastructures (ESFRI) has included in its road map the EMBRC (“European Marine Biological Resource Centre”) infrastructure, which will be led by Stazione Zoologica Anton Dohrn in Napoli (Italy) and will include 12 European Marine Stations from 8 member states and, importantly, the European Molecular Biology Laboratory, whose participation signals the attention that basic biology pays to discoveries that can come from marine organisms.

Science proceeds over long periods, extending known rules, mechanisms and processes to diverse phenomena. This is the linear phase of scientific progress. However, radically different scenarios may develop that impose a change in pre-existing paradigms. Marine science has the potential to initiate such a paradigm shift at the frontier of biology.

Key references

Allen A.E. et al. (2011) Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature, 473: 203-207

Gilbert J. and Dupont C. (2011) Microbial Metagenomics: Beyond the Genome. Annual Review of Marine Science, 3 (1): 347-371

Ullrich-Luter E.M., Dupont S., Arboleda E., Hausen H., Arnone M.I. (2011) Unique system of photoreceptors in sea urchin tube feet. PNAS, 108: 8367-8372

Venter J.C. et al. (2004) Environmental Genome Shotgun Sequencing of the Sargasso Sea. Science, 304: 66-74