Photosynthesis or planktonic respiration?

Abstract

The nutrient-poor (oligotrophic) regions of the open ocean cover 30% of the Earth's surface. Microscopic plants (phytoplankton) living in this habitat account for about 10% of global CO₂fixation¹. Most of this organic production is rapidly respired within a microbial food web dominated by photosynthetic bacteria, heterotrophic bacteria and small (<5 μm diameter) protozoa and algae, with a small amount (about 1% of global co₂fixation) being exported from nutrient-poor upper ocean regions to the interior of the ocean²,³. Thus, on average, photosynthesis exceeds respiration in the sunlit ‘euphotic’ zone of the oligotrophic ocean. This view appears to have been challenged by del Giorgio and co-workers⁴.

Main

Although their conclusion that “…bacterial respiration is generally high, and tends to exceed phytoplankton net production in unproductive systems (less than 70 to 120 μg carbon per litre per day)” is likely to be valid for lakes, it is unlikely to hold in the oligotrophic ocean. An excess of net photosynthesis over respiration is evident in seasonal accumulation of O₂in near-surface waters⁵ at those times when nutrient supply from the interior of the ocean is cut off by vertical stratification. Net photosynthesis is also evident in downward transport (export) of particulate² and dissolved organic matter³ from the euphotic zone to the interior of the ocean.

The conclusion of del Giorgio et al. that the oligotrophic ocean euphotic zone is net heterotrophic was based on analysis of estimates of bacterial respiration and primary production taken from the literature. But a systematic bias in methodology, possibly the consideration of phytoplankton respiration, may account for such a discrepancy.

Both bacterial biomass and bacterial respiration in oligotrophic ocean environments was probably overestimated by del Giorgio et al. Photosynthetic picoplankton can be mistaken for heterotrophic bacteria in conventional epifluorescence counts, leading to an overestimate of the abundance of heterotrophic bacteria in the most oligotrophic waters. For example, photosynthetic bacteria within the genus Prochlorococcus accounted for 31% of total bacterial counts (upper 200 m) in the oligotrophic North Pacific, and the biomass of photosynthetic picoplankton exceeds that of heterotrophic bacteria⁶.

del Giorgio et al. relied on dark O₂consumption in the <0.8-2-μm size fraction to estimate bacterial respiration. but in fact phytoplankton are likely tocontribute significantly to dark oxygen consumption in this size fraction. Respiration is strongly correlated with growth rate in phytoplankton. For phytoplankton with a specific growth rate of 0.7 d⁻¹ typical of open ocean⁷, a specific respiration of 0.4 d⁻¹ is anticipated⁸. This estimate of phytoplankton respiration can be compared with a calculation of the specific bacterial respiration rate of 0.4 d⁻¹ based on a growth rate⁹ of 0.1 d⁻¹ and growth efficiency⁴ of 0.2. Given equal biomass of heterotrophic bacteria and picophytoplankton⁶, it is likely that picophytoplankton account for about 50% of oxygen consumption in the <0.8-2-μm size fraction of oligotrophic ocean waters. as a consequence, heterotrophic bacterial respiration may have been overestimated by 200% in such waters. del Giorgio et al. compared their estimate of “bacterial” respiration with net photosynthesis. As the contribution of phytoplankton to respiration is already included in the net photosynthesis measurement¹⁰, del Giorgio et al. could have counted the contribution of picophytoplankton to respiration twice in their analysis.

In their paper, del Giorgio et al. assumed a respiratory quotient (RQ) of 1.0 CO₂evolved per O₂consumed to convert bacterial respiration from oxygen to carbon equivalents. This RQ is unconstrained by observations for open ocean bacteria, but it is likely to be an overestimate of CO₂evolution from respiration of organic matter that includes proteins and lipids in addition to carbohydrates. Oceanographers typically use a photosynthetic quotient of 1.25 O₂evolved per CO₂assimilated to convert measurements of primary production from carbon to oxygen equivalents¹¹ for comparison with respiration rates measured as O₂consumption. Multiplying the 200% overestimate of heterotrophic bacterial respiration by a photosynthetic quotient of 1.25 leads to an error of 250%.

Cross-system analyses, such as that undertaken by del Giorgio and co-workers, are necessary for clarifying our understanding of the relationship between heterotrophic and photosynthetic metabolism in aquatic systems. However, the conclusion of net heterotrophy of unproductive oceanic systems needs to be tempered, given uncertainty in phytoplankton respiration rates or other possible systematic errors in bacterial respiration and primary productivity measurements.

Reply – del Giorgio & Cole