Extensive prokaryotic maintenance respiration in the sea influenced by osmoregulation

Abstract

Microbial respiration is the major process consuming oxygen in the biosphere. The relative energy demand from growth of biomass or maintenance activities determines the regulation of respiration with impact on how the development of hypoxia and CO2 emissions is controlled. This coupling is crucial for understanding the life history and associated ecological interactions of microorganisms. However, the knowledge of rate and regulating factors of maintenance respiration in the biosphere is limited. In this study, we demonstrated significant relationships in marine field samples where the prokaryotic specific growth rate predicts cell-specific respiration, in accordance with theory from culture models, over a 10-fold salinity range. This enables the first reported direct estimates of maintenance respiration in nature to show a 6-fold variation between 0.12-0.62 fmol O2 cell-1 d-1, comprising 29-72% of prokaryotic specific respiration. The lowest maintenance respiration occurred at salinity close to physiological osmolarity, suggesting osmoregulation as one of the more energy-consuming maintenance activities. A conservative global estimate of maintenance respiration accounted for 66% of the total prokaryotic respiration in the ocean´s mixed layer. This means that maintenance activities dominate the use of the energy generated by prokaryotic respiration in the sea, where osmoregulation is one significant energy consumer. Consequently, maintenance respiration and its regulation must be included in ecological and biogeochemical models to accurately project and manage the development of hypoxia and CO2 emissions from the ocean.

Regulation of marine plankton respiration: A test of models

“…Riverine DOC exceeds the carbon supply from estuarine phytoplankton carbon fixation by 4-fold and explains part of the high plankton respiration levels during winter with negligible phytoplankton production (i.e., baseline respiration, del Giorgio and . Other reports of significant plankton respiration at zero phytoplankton production prevail (Williams and Le, 1998;Du and Shen, 2015), although this was not further discussed by the authors. Thus, riverine DOC can supply coastal respiration with carbon substrates when discharges are sufficient and should be considered together with primary production in coastal areas.…”

“…The influence of riverine discharge is lacking in identified models but shown as a major driver in a Baltic Sea estuary (Vikström et al, 2020). The autochthonous productivity in meso-and eutrophic environments appear to systematically increase plankton respiration, although continued increase (Duarte and Agusti, 1998;Williams and Le, 1998) or levelling off (Hopkinson and Smith, 2005) at higher productivity rates differ between studies.…”

“…Few studies have directly addressed the regulation of plankton respiration. Research with a focus on respiration has been directed toward the trophic balance between pelagic respiration and carbon fixation (Duarte and Agusti, 1998;Williams and Le, 1998;del Giorgio and Duarte, 2002;Williams et al, 2004) and more recently, climate change effects (Lopez-Urrutia et al, 2006;Vazquez-Dominguez et al, 2007;Sarmento et al, 2010;Panigrahi et al, 2013). One study that directly addressed the regulation of bacterioplankton respiration showed a relationship to DOC (Alonso-Saez et al, 2008), and several studies of respiration in Chesapeake Bay also provide valuable results that are relevant to the regulation of plankton and bacterioplankton respiration (Smith and Kemp, 1995;Smith and Kemp, 2001;Smith and Kemp, 2003).…”

“…Complicating the relationship between bacterioplankton respiration and growth, the contribution of maintenance respiration of prokaryotes is probably of a sufficient extent to influence plankton respiration regulation in the field (Carlson et al, 2007;Vikström and Wikner, 2019;Verma et al, 2022;Wikner and Vikström, 2023). This should also apply to other planktonic organisms (e.g., Norberg and DeAngelis, 1997) but is not discussed in a review of zooplankton respiration (Hernańdez-Leoń and Ikeda, 2005).…”

Ecological consequences of climate change in boreal marginal seas

“…Complicating the relationship between bacterioplankton respiration and growth, the contribution of maintenance respiration of prokaryotes is probably of a sufficient extent to influence plankton respiration regulation in the field (Carlson et al, 2007;Vikström and Wikner, 2019;Verma et al, 2022;Wikner and Vikström, 2023). This should also apply to other planktonic organisms (e.g., Norberg and DeAngelis, 1997) but is not discussed in a review of zooplankton respiration (Hernańdez-Leoń and Ikeda, 2005).…”