In the depths

The cold deep sea

For those of us who rarely venture on the surface of the waves, it is difficult to comprehend how big the oceans of the world are. They cover nearly three times as much area of the Earth as does the land. The oceans are a three-dimensional habitat. Their average depth is more than 3 kilometres and the deepest parts, the great ocean trenches, reach a depth of nearly 11 kilometres below the surface. This is much deeper than the largest mountains on the land are tall. Life is found pretty much everywhere in the oceans. Among other things, marine habitats vary with latitude, proximity to land, availability of solid substrates such as rock and depth. There is a great range and variety of ocean habitats.

Humans cannot survive beneath the surface of the sea for long without special equipment. The ocean depths are so outside our experience that it is difficult to judge what parts of its variety of habitats are extreme or not extreme. The availability of water is clearly not a problem for marine organisms and there is sufficient oxygen dissolved in most waters to supply their needs. Temperature is by and large no problem either. The enormous mass of water provides a great deal of thermal buffering. The surface waters are the most variable, reaching 40 °C in the shallow seas of the Arabian Gulf and the Red Sea. The lowest surface temperature is — 1.9°C in polar waters, determined by the freezing point of seawater. In the tropics and at the poles, there is little change in surface temperature with season. Temperate waters are more variable, with temperatures around the United Kingdom reaching 19 °C in September and falling to 2°C in winter. Temperature declines with depth and deep waters below 2000 metres are at a constant 2-4 °C throughout the world.

Light is absorbed by seawater and, even in clear waters, only 1 per cent of the sunlight falling on the surface penetrates to a depth of 50 metres. Photosynthetic organisms are not found below about 100 metres. Most organisms living deeper than this have to rely on food in the form of detritus (dead organisms and other organic debris) drifting down from the surface waters. Pressure increases rapidly with depth and organisms living at the bottom of the oceans have to cope with enormous pressures. How they do so will be covered in Chapter 6.

Until recently, our knowledge of organisms living in the ocean depths has been extremely limited. Scientists trying to sample organ isms from the depths have had to solve the technical difficulties posed by the distance from the surface and the high pressures involved. In the late 1960s, Bob Hessler and Howard Sanders from the Woods Hole Oceanographic Institute began investigating deep ocean beds using a sledge which was towed behind their ship, collecting samples into a net. They found that, rather than the muds of the deep ocean being a virtual desert, as had been previously assumed, they contained large numbers of animals. In the mid1980s, Fred Grassle, of Woods Hole, and Nancy Maciolek headed a team of scientists who spent two years collecting a series of cores from a depth of around 2100 metres off the east coast of the USA. Of the animals they found, 58 per cent were new to science. Each extra kilometre they sampled yielded a new species. Extrapolating from this, they estimated that the ocean depths could contain about 10 million species. This estimate is, however, based on sampling a very small proportion of the ocean bed and some think it is way too high. Others, however, point out that the estimates are based only on the numbers of relatively large invertebrate animals. Microscopic invertebrates, particularly nematodes, also occur in large numbers and most of those that have been recovered from the depths have proved to be new species. Estimates of the numbers of deep sea species thus vary from half a million to 100 million. To put this into context, about 160000 marine species have been described so far and about 1.8 million for the whole Earth. It is clear that the deep oceans provide a substantial proportion of the Earth's biodiversity and that much of it remains to be discovered.

Scientists have also begun to explore the depths using submersible vehicles. Remote operated vehicles (ROVs) are engineered to withstand the high pressure and are controlled by, and send data via, a cable connected to a ship on the surface. In 1995, Japanese scientists succeeded in landing their ROV Kaiko at the bottom of the Mariana Trench in the Philippine Sea. This is the deepest ocean trench in the world and one which would easily accommodate Mount Everest if it were submersed upside down. Even here, the cameras attached to Kaiko soon observed life in the form of sea cucumbers and worms. The life visible on the surface of the mud is, however, little indication of what lies beneath. Samples brought back by Kaiko from the Mariana Trench contained millions of bacteria per gram of mud - much less than would be found in garden soil, but still a reasonably large number.

Both unmanned ROVs and manned submersibles are also changing our view of the great volume of ocean that lies between the ocean floor and the surface waters. Sampling this region with nets only catches a tiny proportion of the animals that live there. Many are too fragile to be transported from the water which supports them. Submersibles such as Deep Rover, a one-person submersible operated by the Monterey Bay Aquarium Research Institute, allow scientists to observe the life of this region directly. Most animals there are transparent and jelly like. Siphonophores belong to the same phylum as jellyfish, but make up colonies of animals which may be as much as 40 metres long. They act like living driftnets, catching particles of food in the water. Bruce Robinson, a scientist at the Monterey Bay Aquarium, describes the midwater as 'a dim, weightless world filled with ragged three-dimensional spiderwebs' and that the animals, and their discarded body parts, are so numerous that 'we now think of this delicate marine life as forming much of that midwater environment.'

Hot vents and cold seeps

In some places, life on the ocean floor does not have to rely on the detritus descending from the surface but can tap other, more unusual, sources of energy. In 1977, scientists from the Woods Hole Oceanographic Institute, exploring near the Galapagos Islands using their ROV Alvin, found the deep ocean vents which had been predicted by geologists. These are areas where material deep within the Earth comes to the surface, forming new seafloor and moving apart the great continental plates which make up the Earth's surface. Water penetrates these vents and emerges superheated, because of the high pressure, to temperatures as high as 350 °C. What was not predicted, however, was that these seemingly inhospitable hydrothermal vents teemed with life. They were surrounded by large numbers of giant tube

figure 2.10 Hydrothermal vent fauna, including clams, crabs and tubeworms. The tubeworms grow up to 1.5 metres tall. Drawing by Jo Ogier.

worms, up to 11.5 metres long, giant clams, crabs and fish (Figure 2.10). More than 400 species of animals have been identified (by 1997), with molluscs, arthropods and annelids being the commonest groups. The tube worms were initially a bit of a mystery, being previously unknown to science. They turned out to be pogonophorans, a previously obscure phylum of animals only discovered in 1900. The pogo-nophorans around the vents are so different from others of the phyla that they are often given their own class or phylum, the Vestimeniferans. Vestimeniferans have no gut or intestinal system and no light penetrates to the depths where the hydrothermal vents are found. What do the tube worms and other animals feed on?

The hot water issuing from the vents is rich in minerals dissolved under high temperature and pressure from rocks beneath the surface. It often contains high concentrations of sulphides. Hydrothermal vents swarm with bacteria (archaea) which live by oxidising the sulphides (mainly hydrogen sulphide) to release their chemical energy. The animals feed on the bacteria or on other animals. The tube worms, and other animals, harbour the sulphur-oxidising bacteria within their tissues, feeding on the nutrients produced by their activities. This was the first community of organisms to be discovered which obtains its energy from chemicals (chemotrophic) rather than sunlight (photo-trophic). Although the water emerges from the vents at very high temperature (over 300°C), it rapidly cools as it moves away to the temperature of the surrounding seawater (about 2°C). The bacteria, however, need to be close to the vents to capture the sulphides before they become too dilute. They are extreme thermophiles and can tolerate temperatures as high as 113 °C. They also need access to oxygen (or to nitrous oxide) dissolved in the seawater surrounding the vents to oxidise the sulphides. The organisms inhabit a fairly narrow zone around the vents where their requirements for sulphides and oxygen can be met. The tube worms are bright red because of the haemoglobin in their blood; this transports not only oxygen (as does our blood), but also sulphides (which is unusual). The animals thus supply their bacterial partners with the chemicals they need. Some vent animals can tolerate temperatures up to about 50 °C, but most animals are associated with waters at temperatures below 30 °C. The hot waters from the vents and the cold waters of the surrounding ocean do not mix well, however, and the animals are exposed both to extremes of temperature and to rapid changes in temperature. They also have to tolerate the high concentrations of minerals, and other toxins, dissolved in the water.

In places, the minerals are deposited to form tall chimney-like structures. Black sulphide-rich water issues from the top of these, giving them the name 'black smokers'. Some organisms live on the walls of the black smokers, where they may be exposed to very high temperatures. The Pompeii worm (Alvinella pompejana), so called because it lives within the rain of volcanic material issuing from the black smokers, is a polychaete worm (an annelid, the same phylum as earthworms) that lives in tubes which it constructs on the outer walls of the chimneys. While the temperature of the water within the chimneys is very high, it rapidly cools when it meets the surrounding seawater. The Pompeii worm, however, lives very close to the scalding water and probes inserted into their tubes have measured temperatures as high as 81°C at the end closest to the chimney and 22°C at their opening. If these temperatures reflect those within the worm itself, this means that the Pompeii worm is the most thermotolerant animal known and one which is exposed to an extraordinary temperature gradient along its body of up to 60 °C.

In 1984, another strange deep-sea habitat was discovered. Erwin Suess of the Research Centre for Marine Geosciences in Kiel, Germany, also using the ROV Alvin, observed wedges of mud in the form of ridges accumulating where the Juan de Fuca tectonic plate slides beneath the North American plate off the coast of Oregon. These were dotted with stone chimneys formed of minerals from plumes of water and gas issuing from the seabed. However, unlike the hydrothermal vents, these waters were cold, giving them the name 'cold vents' or 'cold seeps'. If the temperature is low enough, the methane issuing from these seeps becomes trapped within an icy cage of water molecules, forming methane hydrates which look like lumps of dirty ice. Methane hydrates are also found on land in places in the Arctic. These hydrates have been shown to occur throughout the oceans of the world in enormous quantities and it is thought that the world's methane hydrate deposits contain twice as much carbon as all known coal, oil and natural gas deposits put together. They could be an important energy resource when other fossil fuel reserves are exhausted, if the problems of harvesting them can be overcome. These methane deposits are thought to have been formed by microorganisms decomposing the organic material in ocean sediments.

Melting of the methane hydrate releases not only methane and water but also hydrogen sulphide and ammonia. These chemicals provide an energy source for dense communities of chemotrophic bacteria, which, in turn, provide food for animals including clams and tube worms. The only animal which actually lives within the methane hydrate is the 'ice worm', Hesiocaeca methanicola, a species of polychaete worm. These worms create a current of water which gradually wears away the ice and form burrows in which they live, feeding on the bacteria. The methane ice is, however, an unstable place to live, since it melts above 6 °C and a small rise in temperature can cause it to disappear.

The underworld

Until about the late 1980s, most scientists believed that life was restricted to the top few metres of the soil or ocean sediments. As depth increased, nutrients became sparse and so did organisms. The few reports of organisms being recovered from great depths within the Earth were dismissed as contamination with material from the surface layers. Two technical developments changed this view. The first was the development of drilling techniques which gave confidence that cores could be retrieved from depth without contamination. Samples were recovered using a diamond-studded drill bit which headed a great length of rotating steel pipe from a drilling derrick. A concentrated tracer material was added to the lubricating fluid so that when the core of rock was removed any contaminated material could be identified and cut away to leave a pristine sample of rock from deep within the Earth. The second development was the advent of techniques for identifying microorganisms without having to grow them in culture. All organisms contain DNA and their presence can be revealed by dyes which either stain DNA directly or can be attached to nucleic acid probes. By varying the nucleic acid probe, the presence of different types of microorganism can be demonstrated.

The first scientists to use these techniques were involved in the Subsurface Science Programme of the US Department of Energy (DOE). They were interested in the possibility that, if organisms existed in the depths of the Earth, they might degrade organic pollutants and help maintain the purity of groundwater or, rather less usefully, degrade the containers in which the DOE was proposing to deposit the radioactive waste from nuclear facilities. They demonstrated the presence of many different types of microorganisms in rocks at depths down to 500 metres beneath the surface. Since then, microbes have been discovered in many different types of rocks and deep within ocean sediments. The record depth at which life has been found is at the bottom of a South African gold mine, 3.5 kilometres below ground. Pressure and temperature increase as you go deeper into the Earth. Bacteria from hydrothermal vents can grow at 110 °C and some scientists think that subsurface bacteria could withstand temperatures as high as 150°C. This would allow organisms to exist to depths of about 7 kilometres beneath the seafloor and to 4 kilometres below the surface of the land. Although the organisms are often sparsely distributed, this is such an enormous volume that it has been estimated that the total biomass of deep subsurface organisms exceeds that of those living on, or just below, the surface.

Bacteria are the most numerous of these subsurface organisms, but there are also fungi and protozoa. Some 10000 strains of microorganism have been isolated from subsurface cores. Each gram of rock contains anything from 100 bacteria to 10 million bacteria (compared with more than one billion per gram in agricultural soils); ocean sediments contain even higher numbers. The protozoa feed on the bacteria, forming part of a simple subterranean food chain, but what do the bacteria feed on? Sedimentary rocks are formed from sands and from ocean, river or lake sediments that have organic material trapped within them. Microbes living in pores within the sediments can utilise these ancient nutrients and grow. As sedimentary rocks are buried more deeply, they become increasingly compacted and their pores filled with minerals. The distribution of microorganisms is thus likely to become more patchy, condensed into the remaining pores and concentrations of nutrients. The bulk of the Earth's crust, however, consists of igneous rocks, such as granite and basalt, which are solidified from molten magma. These rocks were too hot to support life when they were first formed; the organisms which inhabit cracks and fissures within the rocks are carried there by the groundwater flowing through them. Subsurface bacteria do not just rely on nutrients trapped within the rock or carried there by groundwater. Some are chemo-trophs, deriving their energy from the oxidation of iron or sulphur compounds and building organic material directly from the carbon dioxide and hydrogen gas dissolved in the rock. These bacteria excrete organic compounds which are then utilised by other types of bacteria. These ecosystems based on chemotrophic bacteria are completely independent of material and solar energy from the surface. They have been referred to by some scientists as 'SLiMES' (subsurface lithoautotrophic microbial ecosystems). Some of these communities of organisms have been isolated from the surface for a long time and are at least several million years old. Nutrients are in short supply in most parts of the deep subsurface and the organisms are likely to grow very slowly indeed, perhaps reproducing once every few hundred years. The bacteria are typically very small, reflecting the low availability of nutrients.

The discovery of life beneath the surface of the Earth has profound implications for our understanding of many of the processes which occur there. Changes in the deep subsurface, rather than being due to purely physical and chemical transformations, may also involve biological processes. Bacteria may be involved in the concentration of minerals, such as gold, into seams and methane-producing bacteria could be responsible for forming natural gas deposits. It has even been suggested by Tom Gold of Cornell University, in a controversial theory, that the world's oil deposits are formed by the activity of subsurface microorganisms, rather than from the remains of ancient plants and animals. This would mean that the formation of oil is a continuing process and that, rather than oil reserves being finite, they are being continually renewed. Many of the bacteria may break down organic material and be useful in the cleaning of contaminated soils and groundwater.

In places, material from the underworld makes an appearance at the surface. Bacterial flocks emerging from some deep sea vents originate from SLiMEs and, as we have seen, minerals emerge from hydrothermal vents and cold seeps. Material from the deep makes a dramatic appearance on land in the form of volcanoes. The violent eruptions of lava and ash destroy any life with which they come into contact, but, eventually, the eruptions cease, the volcanic material cools and it is colonised by organisms. Rather less violent are hot springs formed by groundwater or rainwater which has been heated through contact with lava and forced to the surface. The scaldingly hot water can nevertheless support the growth of extreme thermophilic bacteria and cyano-bacteria (see Chapter 4). Volcanic activity can even make some otherwise inhospitable environments capable of supporting life. Mount Erebus on Ross Island in the Antarctic is an active volcano. Around the edge of the volcano, the temperatures are high enough to melt the ice but low enough to support the growth of moss, algae and other organisms.

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