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A Latitudinal Gradient in the Prokaryote to Eukaryote Ratio Inmarine

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A Latitudinal Gradient in the Prokaryote to Eukaryote Ratio Inmarine Not to be cited without prior reference to the author ICES CM 2008/A:02 1 A latitudinal gradient in the underpin ocean food webs and drive global prokaryote to eukaryote ratio in biogeochemical cycles. At the same time, by marine microbes virtue of astronomical numbers, mobile genetic elements, and seemingly facile cellular dispersion, microbes also shape William K.W. Li ecosystems by information flow, which Bedford Institute of Oceanography records idiosyncratic characteristics and Dartmouth, Nova Scotia, Canada, B2Y 4A2 historical contingencies. The scales of space and time at which Email: [email protected] individual microbial cells interact with their environment (living and non-living) are short, Abstract but we need to discern lawlike behaviours for The coexistence of the three domains of life microbially-influenced phenomena such as in marine plankton indicates extreme harvest fisheries and climate change which evolutionary and ecological diversity in the have a much larger scale. The problem may pelagic realm. The dichotomy between be viewed as a reordering of hierachical levels prokaryotes (domains Bacteria and Archaea) according to spatial and frequency and eukaryotes (domain Eukarya) is characteristics (2). The concept of an paradigmatic but also burdened by semantics ecological geography of the sea (3) is an and mythology. Fundamental debate on the exemplar of spatial reordering. This validity of the term “prokaryote” centres on parsimonious partition of the world oceans molecular organisation and evolution, but into non-overlapping provinces defined by little consideration is given to ecology. Here, physical and biological oceanography an empirical examination is made of the achieves the necessary change in context ecological dichotomy of these microbes in the required to constrain variable local behaviour. surface ocean. Extensive observations of cell As a nested hierarchical element, each abundance in numerous contrasting ocean province physically contains all lower level provinces indicate that the numerical ratio of spatial elements, and in turn can be prokaryotes to eukaryotes decreases aggregated with other provinces to the highest poleward. The ecological balance between level which is the global ocean. these microbes which have different types of Microbes, the low level biological entities cellular architecture may therefore be for which we seek pattern at a high level, can organised by biogeographic processes that act be variously ordered, for example by trophic as low-pass filters integrating the features of mode, size class, ecological function, or finer taxonomic units. taxonomy (4). In evolutionary terms, the deepest distinction amongst microbes is at the Hierarchical organisation in microbial domain level: Bacteria, Archaea, Eukarya. oceanography The dichotomy between eukaryotes and Marine microbes are polyphyletic unicells prokaryotes (i.e. non-eukaryotes) is a long- which dominate the living ocean by their standing paradigm (5) which is now known to abundance, biomass, surface area, and have no basis in deep phylogeny (6) nor production (1). By transforming energy and foundational roots from which a single chemical substrates in a multitude of inclusive hierarchical tree of life might appear metabolic processes, marine microbes to emerge (7). Yet the dichotomy arguably Not to be cited without prior reference to the author ICES CM 2008/A:02 2 retains considerable utility, rhetorical or Fig. 1. Average abundance of microbial otherwise (8). Notwithstanding fundamental prokaryotes in biogeochemical provinces. The dahed line is a LOWESS fit. differences at the molecular level, Bacteria and Archaea share many phenotypic features Microbial eukaryotes comprise plastidic perceived to be important in the structuring of and aplastidic protists in various size classes. ecosystems, for example cell size, metabolic As a group, they number in the thousands per capabilities, and elemental stoichiometry. ml (average 5.5 ± 4.9, range 1.0 – 18.6), being Here, we explore the abundance of more abundant in provinces at mid latitudes in prokaryotes and eukaryotes in pelagic the North Atlantic (Fig. 2). The highest microbial communities at the megameter abundance of planktonic microbes was scale of ocean provinces. We find that observed in the Humboldt Current Coastal prokaryotes always outnumber eukaryotes in Province (HUMB) off Chile at an surface waters but the imbalance is approximate mean latitude of 22oS, which is a progressively accentuated from high to low location of intense upwelling driven by the latitudes, leading to a view that the global eastern boundary current. distribution of marine microbes is shaped not only by energy, chemicals and metabolites, 20 ) but also by genes. -1 15 cells mL Microbial abundance in the surface ocean 3 We estimated microbial abundance in 5420 10 surface seawater samples collected from 29 biogeochemical provinces over a span of 19 5 years. Prokaryotes comprise non- (10Eukaryotes photosynthetic bacteria and archaea, together 0 -80-60-40-200 20406080 with the oxygenic photoautotrophic Latitude cyanobacteria Synechococcus and Fig. 2. Average abundance of microbial Prochlorococcus. As a group, they number in eukaryotes in biogeochemical provinces. The the millions per ml (average 0.72 ± 0.47, dashed line is a LOWESS fit. range 0.22 – 2.5), being more abundant in provinces at low latitudes than at high The prokaryote to eukaryote abundance latitudes (Fig. 1). ratio emerges as a high level pattern formed by the relationship between two separately 3.0 ) nested groups. The ratio has a magnitude of -1 2.5 order 2 (average 240 ± 148, range 46 – 518) 2.0 and displays a strong poleward decrease in cellsmL 6 provinces away from the equator in both 1.5 hemispheres (Fig. 3). Notably, the 1.0 exceptionally high abundances of both kinds 0.5 of cells in HUMB form an unexceptional ratio Prokaryotes (10 that conforms to the broad unimodal 0.0 -80-60-40-200 20406080 latitudinal pattern. Latitude Not to be cited without prior reference to the author ICES CM 2008/A:02 3 latitudes (10). Meta-analysis suggests that 600 strong latitudinal gradients in richness are 500 mitigated by small body mass (11), but recent 400 direct assessments of marine prokaryotes 300 confirm a poleward decrease in richness of bacterial operational taxonomic units (12,13). 200 The pattern for marine microbial eukaryotes 100 as a group is less clear because species Prokaryotes : Eukaryotes 0 richness for component taxa such as -80-60-40-200 20406080 eukaryotic phytoplankton, calcareous Latitude nanoplankton, foraminefera, and radiolaria Fig. 3. Average abundance ratio of prokaryotes to are variously distributed with respect to eukaryotes in biogeochemical provinces. The dashed line is a LOWESS fit. The solid line is a latitude (14, 15). Gaussian fit. Most eukaryotes are larger in size than prokaryotes; thus the numerical balance The ratio of prokaryotes to eukaryotes between them might be seen as an expression The ordination of the prokaryote to of the allometric relationship linking body eukaryote ratio according to geographic mass (M) and abundance (N). Across pelagic latitude is strikingly clear. Apparent marine communities and across trophic levels, symmetry of this ratio about the equator the scaling exponent is close to -1, thus N~M-1 suggests that this is not a simple (16,17). Integral calculus dictates that 96% of physiographic pattern since the oceans are the number of cells in the microbial plankton asymmetrically configured in opposite (0.4 – 200 µm) can be expected in the hemispheres. It would seem that the balance picoplankton size class (0.4 – 2 µm), which between microbial groups evidenced at the contains all the prokaryotes, but also some level of ocean provinces is not a random very small eukaryotes (18). If we apportion outcome but a pattern based on biogeographic 1% of the picoplankton to picoeukaryotes, process (9). The defining characteristic of then a size-based inference of 19 (= 95/5) for provinces is the resistance of the water the prokaryote to eukaryote ratio would column to vertical mixing, but the Brunt- obtain. This seems to be a reasonable null Väisälä frequency which measures this condition as it is the same order as the resistance is not a simple function of latitude observed minumum (Fig. 3). Being small in (3). Thus the microbial pattern is likely to be the pelagos confers putative advantages and conflated in many environmental correlates, encumbers putative disadvantages, and such as temperature, salinity, irradiance, phytoplankton should seemingly evolve daylength, nutrients, wind stress, towards picoplankton size (19). Evidently, stratification, productivity, grazers, and other almost all arguments made strictly on the factors. basis of cell size fall somewhat short without The multifaceted nature of latitude renders biological nuance (20). It remains to explore it a useful principal component in the the progressive increase of prokaryote ordination of biodiversity. The earliest dominance towards the equator beyond the recognized macroecological pattern is the allometric constraints. general decrease in taxonomic richness of A starting point is to recognise that many organism groups from low to high prokaryotes have chromosomes with a single Not to be cited without prior reference to the author ICES CM 2008/A:02 4 origin of replication, which thus limits unicellular eukaryotes indicates the state of genome size because the replication rate microbial genetic diversity. Horizontal
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