Impact of cable bacteria on biogeochemical cycling in sediments of a seasonally hypoxic marine basin

Abstract

Oxygen is a key element for life on earth. It can be taken up by ocean waters via air-sea gas exchange, but is also formed through photosynthesis by phytoplankton in the photic zone. In seawater, oxygen can be consumed through aerobic respiration, where it is used as an electron acceptor in the breakdown of organic matter, in a process known as remineralisation. Dissolved oxygen is necessary for the respiration and metabolism of many marine organisms, several types of which are sensitive to concentrations below thresholds as high as 91 µM O2; yet an oxic water body is defined as containing at least 62.5 µM (2 mg L-1) oxygen. An increased oxygen demand or reduction in oxygen supply can result in oxygen-deficient or hypoxic conditions (< 62.5 µM) and may eventually lead to oxygen depletion or anoxia. Hypoxia and anoxia in coastal waters can occur naturally, mainly affecting water bodies in which water exchange and circulation are restricted. However, low oxygen conditions are becoming increasingly prevalent in the bottom waters of many coastal systems, as a direct consequence of eutrophication, caused by human land-use practices. Increased nutrient input from agricultural run-off and anthropogenic waste disposal can lead to increased primary production in surface waters, where a consequent increase in oxygen demand upon sinking of this organic matter into deeper waters can eventually exceed the supply of dissolved oxygen. Oxygen is the most energetically-favourable electron acceptor for microbial respiration in sediments, but in its absence, a cascade of alternative electron acceptors is available for anaerobic respiration. Anaerobic mineralisation dominates in most coastal sediments due to the high organic matter supply. Iron and manganese-(oxyhyr)oxides can serve as electron acceptors for microbial respiration in the absence of oxygen. Many trace metals can be associated with iron and manganese minerals. Variations in trace metal enrichments in coastal surface sediments can be used as indicators of hypoxic and anoxic conditions in these environments. Iron and manganese cycling also plays a pivotal role in nutrient cycling in coastal environments. Increased availability of nutrients like phosphorus, for autotrophic metabolism, can lead to enhanced primary productivity in coastal surface waters. Under low oxygen concentrations, phosphorus is released from surface sediments, liberated from iron- and manganese-(oxyhydr)oxides into overlying waters. Sedimentary phosphorus cycling is very redox-sensitive and phosphorus recycling can be pivotal to the maintenance of low oxygen conditions in coastal systems, by fuelling primary production and organic matter supply to bottom waters. Furthermore, sulphur-oxidising cable bacteria can influence redox conditions, as well as elemental recycling and burial in coastal sediments. Cable bacteria have been observed to link sulphide oxidation to the reduction of oxygen over centimetre-long distances in the sediment via electrogenic sulphur oxidation (e-SOx). Cable bacteria induce a range of secondary biogeochemical reactions including dissolution and precipitation of minerals. For example, proton generation associated with anodic sulphide oxidation can lead to dissolution of sulphide and carbonate minerals and mobilisation of calcium, iron and sulphate ions to the pore water. Cable bacteria have been detected in many aquatic systems worldwide and are now known to occur in environments ranging from hot vents, freshwater and marine sediments, to mangroves and even aquifers.