The hadal biosphere: Recent insights and new directions

Abstract

The hadal zone is the deep ocean with depths exceeding 6000 m. With an area approximately equal to the size of Australia, but constituting the deepest 45% of the vertical depth of the global ocean, it should come as no surprise that the hadal zone is the last great frontier of the ocean science. Historically, the hadal trenches are believed to have limited activities of life, microscopic or macroscopic, due to the extreme environmental conditions such as high hydrostatic pressure, lacking of sunlight and food supply, as well as frequent subduction-zone earthquakes. However, seminal discoveries have been made recently by scientists working at hadal trenches on microbial and faunal community structure, abundance, diversity, and mechanisms for endemism, speciation and adaptation, likely regulated by a myriad of specific geological, physical, and chemical factors of the hadal zone, forming the so-called “hadal biosphere”. These discoveries ignited a new wave of hypotheses and theories on organismal metabolism, energy acquisition, and the origins of life on Earth. Here, we review the recent development in understanding the hadal biosphere and discuss future directions on hadal biosphere research.

Introduction

The hadal zone, comprised primarily of troughs and trenches with depth greater than 6000 m, represents the deepest marine habitats with an area approximately equal to the size of Australia (HADES, 2016; Jamieson et al., 2010). Although covering only 1–2% of marine benthic area, the hadal zone constitutes the deepest 45% of the vertical depth of the global ocean, suggesting their great significance in the ocean ecosystem (Jamieson, 2015, Jamieson, 2011, Jamieson et al., 2010).

The hadal zone is featured with extreme physical-chemical conditions, including low temperature, lack of sunlight and phototrophic primary production, as well as frequent subduction-zone earthquakes (Jamieson et al., 2010, Taira et al., 2005). In addition, the hadal environments are topographically isolated from upper oceans, and exhibit extremely high hydrostatic pressure (Jamieson et al., 2010, Nunoura et al., 2016). Moreover, multiple sources of organic matter inputs and special topography of the trenches make the hadal zone “hot spots” of organic matter deposition in the deep ocean (Ichino et al., 2015, Jamieson et al., 2010). Strong large-scale deep-water currents flowing through hadal trenches (Kawabe and Fujio, 2010, Siedler et al., 2004) and active tectonic activities (Itou et al., 2000, Oguri et al., 2013) redistribute organic matter in different parts of hadal trenches, resulting in highly heterogeneous habitats within the hadal zone. The special environmental conditions support a unique trench ecosystem, constituting the so-called hadal biosphere (Jamieson and Fujii, 2011, Jamieson and Fujii, 2011, Nunoura et al., 2015).

Indeed, recent studies have revealed abundant organisms in hadal trenches (Danovaro et al., 2002, Schmidt and Arbizu, 2015), and many special phenomena of life have been found. For example, “supergiant” amphipods have been discovered in the hadal area, with body length ranging from 102 to 290 mm (Jamieson et al., 2013). Moreover, trench communities exhibit highly endemic distributions, structured by either topography, hydrography, surface primary production, or a combination of these factors (Fujii et al., 2013, Gallo et al., 2015, Itoh et al., 2011, Jamieson and Fujii, 2011, Jamieson and Fujii, 2011, Jamieson et al., 2011). It has been suggested that special molecular mechanisms may exist by the organisms in the hadal zone to cope with low temperature, high hydrostatic pressure and other extreme environmental factors, by synthesizing piezolytes such as trimethylamine N-oxide (TMAO) to stabilize proteins (Gillett et al., 1997, Jamieson et al., 2010, Lidbury et al., 2014, Ma et al., 2014, Martin et al., 2002, Yancey et al., 2014). These findings support the existence of the hadal biosphere.

There have been reviews on research progresses in hadal science (Jamieson et al., 2010, Jamieson, 2011). The first book dedicated specifically to hadal science has been published that covers a broad range of topics about the hadal zone (Jamieson, 2015). However, existing reviews were mainly focused on the fauna communities, with less emphasis on microbial community and ecology. On the other hand, with the establishment of several international collaborative programs in trench exploration, e.g. HADal Environment and Educational Program (HADEEP) and the Hadal Ecosystem Studies (HADES) program, publications on hadal biosphere and ecology have increased drastically in recent years (HADEEP world press, 2016; HADES, 2016; Jamieson et al., 2009). After the first international symposium on hadal zone, Trench Connection 2010 (Jamieson and Fujii, 2011, Jamieson and Fujii, 2011), an international summit on hadal science and technology was successfully held during June 2016, in Shanghai, China, at which time up-to-date results on scientific exploration of hadal trenches and technological innovations were presented. This review aims to sum up the recent achievements in exploring the hadal biosphere and discuss future research directions in hadal science.