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Microbial ecology of the South Atlantic Subtropical Gyre: a state-of-the-art review of an understudied ocean region

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Understanding the dynamics of microbial plankton communities, their metabolic processes, and taxonomic composition in oligotrophic ocean basins has been one of the central tasks of contemporary marine microbial ecology and one of the main challenges in a changing global ocean. However, despite its ecological importance, the South Atlantic Subtropical Gyre (SASG) remains poorly understood in relation to marine microbes, which comprise the major drivers of biogeochemical cycles and the largest carbon sink to the deep ocean. This review presents the state of the art of microbial ecology in the SASG, including the adjacent oligotrophic region, the Southwest Atlantic Ocean (SWAO). We have also addressed the theoretical and methodological trends in this field since the 1970s, focusing on the main milestones that led to the more-detailed current knowledge of the role of oligotrophic gyres in the global carbon cycle. Finally, we discussed the general patterns of microbial community composition in the SASG, focusing on their potential responses to environmental factors. In spite of increasing efforts to investigate this region, SASG is among the least known oceanic provinces, which has hampered the debate over whether the oligotrophic ocean acts as a sink or source of CO2 into the atmosphere.
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Ocean and Coastal Research 2021, v69:e21027 1
Microbial ecology of the South Atlantic Subtropical Gyre: a
state-of-the-art review of an understudied ocean region
Luciana Rocha Frazão1, Silvana Batista Penninck1, Luan Sayeg Michelazzo1, Gelaysi Moreno1,2 , Claudia
Guimarães1, Rubens M. Lopes1, Camila Negrão Signori1,*
1 Departamento de Oceanograa Biológica, Instituto Oceanográco, Universidade de São Paulo, Praça do Oceanográco, 191.
05508-120. São Paulo, Brazil
2 Departamento de Física, Universidad de Moa, Avenida Calixto García Iñiguez #15, entre Av. 7 de Diciembre y Calle Reynaldo Lata
Rueda, Rpto, Caribe, Moa, Holguin, cp83330, Cuba
* Corresponding author: csignori@usp.br
Submitted: 27-Nov-2020
Approved: 01-Sep-2021
Editor: Hugo Sarmento
INTRODUCTION
Microbial plankton is an essential component of
marine ecosystems because of its key role in pelagic
food-web dynamics and oceanic biogeochemical
cycles, including the transport of carbon to the deep
ocean (Azam et al., 1983; Cho and Azam, 1990; Gasol
et al., 2008) and xation of an important fraction of
the total atmospheric carbon and nitrogen (Worden
et al., 2015; Logares et al., 2020).
Marine microbes include a diverse class of het-
erotrophic and autotrophic prokaryotes as well as
unicellular eukaryotes (picoeukaryotes), with sizes
ranging from 0.2 μm to 2.0 μm (Sieburth et al., 1978;
Fuhrman, 1999). All these microbes, called picoplank-
ton, have large population sizes, short generation
times, and nearly unfathomable levels of aquatic
biodiversity (Whitman et al., 1998; Thompson et al.,
2017).
Bacteria and Archaea are the two domains of het-
erotrophic prokaryotes that, due to their ubiquity,
abundance (on the order of 106 cells ml–1), high func-
tional diversity and metabolic plasticity, comprise
the majority of the biomass in the oceans (Fuhrman
et al., 1989; DeLong, 1992). Although these two do-
mains dier in some fundamental aspects of their
metabolic features, they have been conventionally
referred to as ‘bacteria’ in prior studies. So, here we
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the terms of the Creative Commons license.
Ocean
and Coastal
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http://doi.org/10.1590/2675-2824069.20026lrf
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ISSN 2675-2824
Understanding the dynamics of microbial plankton communities, their metabolic processes and taxonomic composition
in oligotrophic ocean basins has been one of the central tasks of contemporary marine microbial ecology and one
of the main challenges in a changing global ocean. However, despite its ecological importance, the South Atlantic
Subtropical Gyre (SASG) remains poorly understood in relation to marine microbes, which comprise the major drivers of
biogeochemical cycles and the largest carbon sink to the deep ocean. This review presents the state of the art of microbial
ecology in the SASG, including the adjacent oligotrophic region, the Southwest Atlantic Ocean (SWAO). We have also
addressed the theoretical and methodological trends in this eld since 1970s, focusing on the main milestones that led to
the more-detailed current knowledge of the role of oligotrophic gyres in the global carbon cycle. Finally, we discussed the
general patterns of microbial community composition in the SASG, focusing on their potential responses to environmental
factors. In spite of increasing eorts to investigate this region, SASG is among the least known oceanic provinces, which
has hampered the debate over whether the oligotrophic ocean acts as a sink or source of CO2 into the atmosphere.
AbsTRACT
Descriptors: Marine Microbes, Bacterial Production, Biogeochemical Cycles, Oligotrophic Oceans, Pelagic System.
Microbial ecology of the South Atlantic Gyre
Ocean and Coastal Research 2021, v69:e21027 2
Frazão et al.
use the terms “bacteria” and “bacterial production’ as
a collective term referring to bacteria and archaea.
The autotrophic picoplankton includes two main
groups, photosynthetic cyanobacteria and the single
picoeukaryotes, which may account for up to 64% of
the total carbon biomass in oligotrophic open waters
(Fogg, 1995).
The ecological and biogeochemical processes in
the oceans are dependent on these microbial interac-
tions, which comprise the major drivers of global bio-
geochemical cycles (Falkowski et al., 2008; 2012). The
role of bacteria in marine ecosystems consists largely
of consumption of dissolved organic matter, mainly
as dissolved organic carbon (DOC) derived from pri-
mary production; the bacteria convert the dissolved
carbon fraction into particulate organic matter by
incorporating it (Fuhrman and Azam, 1980; Azam
et al., 1983). Through this process, carbon that was
theoretically inaccessible to heterotrophic organisms
is reintroduced into food webs by microbes, mak-
ing it available to higher trophic levels and the deep
ocean, illustrating the fundamental role that bacteria
play in the microbial loop (Azam and Malfatti, 2007;
Pomeroy et al., 2007).
Understanding the dynamics of microbial plank-
ton communities, their taxonomic composition and
their metabolic processes has been one of the central
tasks of contemporary marine microbial ecology and
a main challenge in better understanding the role
of microbes in a changing global ocean. During the
last ve decades, the growing eorts in this area have
been impelled mainly by technological advance-
ments and improvements that resulted in the nd-
ings that have led to the well-established concepts
regarding the marine food web and carbon ow.
Most recent approaches have yielded new insights
into the role of heterotrophic bacterial production
in oligotrophic oceans and in the biological carbon
pump, and have also driven the development of new
theories, such as the recently proposed microbial car-
bon pump (Jiao et al., 2014; Legendre, 2015; Zhang
et al., 2016).
The implications of global changes for the bac-
terial community and carbon sinks have been dis-
cussed (Morán et al., 2015; Huete-Stauer et al., 2016;
Allen et al., 2020) and studies concerning marine mi-
crobial ecology in open ocean basins and subtropical
oligotrophic gyres have assumed new importance.
The subtropical gyres, because of their immense
size (~ 40% of the surface of the earth) play a signi-
cant role in the global carbon cycle and in sequester-
ing atmospheric CO2 through physical and biologi-
cal processes (McClain et al., 2004; Brix et al., 2006).
Therefore, understanding the interactions between
these two processes within the subtropical gyres is a
central task for determining the magnitude and vari-
ability of the carbon exported from the surface to the
deep ocean, as well as the CO2 exchange between the
atmosphere and the ocean (Signorini et al., 2015).
The South Atlantic Subtropical Gyre (SASG), cen-
tered at approximately 50°W and 30/40°S, is a distinct
biogeochemical province, with unique physical and
biological characteristics relative to adjacent regions
(Longhurst, 2010; Signorini et al., 2015). This anticy-
clonic gyre of approximately 4,500 km diameter is
bordered by a number of major surface ocean cur-
rents and by one of the most oligotrophic areas in the
entire ocean on the Brazilian continental shelf (Alves
Junior et al., 2015), the Southwest Atlantic Ocean
(SWAO) (Figure 1). Despite its ecological importance,
the SASG remains little studied compared to other
ocean basins.
In this review, we address the state of the art of
microbial ecology in the SASG, including the oli-
gotrophic adjacent region (SWAO). We also briey
address methodological trends and conceptual ad-
vances in this eld, which have led to current well-
established models of carbon ows in oligotrophic
pelagic ecosystems, and the need for understanding
whether the oligotrophic ocean is predominantly
net autotrophic or heterotrophic. Finally, we discuss
the general patterns found in the SASG based on the
literature review, focusing on the mechanisms that
shape microbial metabolism in this region.
MARINe MICRObIAl eCOlOgy - MeThODOlOgICAl
TReNDs AND CONCepTUAl ADvANCes
Initially, in an attempt to quantify research con-
tributions to marine microbial ecology over the last
ve decades, we searched for articles published
in peer-reviewed and indexed journals from 1974
through 2020 by the Web of Science portal (www.
webofscience.com). The rst step of our search was
conducted by crossing the terms “bacterioplankton”,
“marine bacteria”, “microbial plankton”, “heterotrophic
bacteria” or “marine bacterial production”, with the
Microbial ecology of the South Atlantic Gyre
Ocean and Coastal Research 2021, v69:e21027 3
Frazão et al.
Figure 1. Schematic representation of major current systems
that aect the South Atlantic Subtropical Gyre, and the ve major
biogeochemical provinces of the Atlantic Ocean: North Atlantic
Drift Province (NADR), North Atlantic Tropical Gyre (NATL), Western
Tropical Atlantic (WTRA), South Atlantic Subtropical Gyre (SASG)
and the South Subtropical Convergence (SSTC). Data were plotted
in Ocean Data View (Schlitzer, 2020).
keywords regarding to the main methods that con-
tributed to the evolution of marine microbial ecology
science: “epiuorescence microscopy ”, or “thymidine”,
or “leucine”, or “ow cytometry”, or “omics” (“metage-
nomics”, “metatranscriptomics”, “metaproteomics”,
“metabolomics”, or “metabarcoding”). Since the pio-
neering work of Pomeroy (1974) was the starting
point of this review, the sequential search included
publications from 1974 through 2020. In a second
step, to select only those studies concerning micro-
bial ecology in marine environments, we conducted
a new screening through a search of keywords in the
title, and when this was not sucient, by reading the
publication abstract. Our compilation resulted in a
total of 758 studies published in marine microbial
ecology. However, the rst published record on the
Web of Science portal dates only from 1978.
In an attempt to provide an overview of con-
ceptual advances that have led to current well-
established models of carbon ows in oligotrophic
pelagic ecosystems, as well as the current debate
over whether the oligotrophic ocean is predominant-
ly net autotrophic or net heterotrophic, we provided
a timeline highlighting the theoretical and method-
ological milestones over the last ve decades (Figure
2). For this, we also considered the relevant studies in
this eld that were not registered in our search. In ad-
dition, for an overview of methodological trends, we
compiled the results from our search by the annual
number of publications involving each of the main
methods (Figure 3 and Table S1). The main advances
in microbial ecology from a historical perspective are
addressed below.
MICRObIAl eCOlOgy IN OlIgOTROphIC OpeN OCeAN bA-
sINs - A hIsTORICAl peRspeCTIve
From the rst perception of the high abundance
of bacteria in marine environments to the current
post-genomic age, great leaps in marine microbial
ecology since the late 1970s have dramatically in-
creased our knowledge in this area, which has be-
come an extremely dynamic eld of research in the
last ve decades. This exponential rate of progress,
closely related to the development of technologies
and advancement of precision methods, has led to
the current high level of understanding of key ocean
processes, including bacterial production (BP), respi-
ration (BR), growth eciency (BGE) and carbon ow
through trophic interactions.
After the initial perception of the high abundance
of bacteria in marine environments using the epiuo-
rescence microscope and uorescent dyes (Hobbie
et al., 1977; Porter and Feig, 1980), the introduction
of radioactive-isotope methods for measuring het-
erotrophic bacterial production (Fuhrman and Azam,
1980; 1982; Kirchman et al., 1985) inaugurated a
new era in studies of microbial dynamics in aquatic
environments.
Some early studies using the 3H-thymidine and
3H-leucine incorporation methods also investigated
the coupling between BP and phytoplankton prima-
ry production (Hobbie and Cole, 1984; Kirchman et
al., 1989). These rst investigations were conducted
in coastal waters (Pomeroy and Deibel, 1986), inner
shelf regions (Fuhrman et al., 1985; Cho and Azam,
1988), estuarine plumes (Ducklow and Kirchman,
1983; Kirchman and Hoch, 1988; Malone and
Microbial ecology of the South Atlantic Gyre
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Frazão et al.
Ducklow, 1990) and upwelling regions (McManus
and Peterson, 1988) of the North Pacic and North
Atlantic. Overall, the observations reported in these
studies indicated changes in the microbial commu-
nity along the open ocean to the coastal gradient, i.e.,
that bacterial biomass and activity were highest near
the coast, tending to comprise <20% of the phyto-
plankton biomass and the total particulate organic
carbon. However, the rst measurements of BP in oli-
gotrophic open oceans, conducted in the euphotic
Figure 3. Annual number of citations of each methodology approach resulting from a search for publications on marine microbial ecology
by the Web of Science website, from 1974-2020. The keywords "epiuorescence microscopy, 3H-thymidine, 3H-leucine, ow cytometry,
metagenomics, metatranscriptomics, metaproteomics, metabolomics and/or metabarcoding were crossing with “bacterioplankton, “marine
bacteria”, “microbial plankton”, “heterotrophic bacteria” or “marine bacterial production”.
Figure 2. Timeline including the theoretical and methodological milestones over the last ve decades (1974-2020) that led to current well-
established models of carbon ows in oligotrophic pelagic ecosystems, and the need for understanding whether the oligotrophic ocean is
predominantly net autotrophic or net heterotrophic.
Microbial ecology of the South Atlantic Gyre
Ocean and Coastal Research 2021, v69:e21027 5
Frazão et al.
zone of the Sargasso Sea and North Pacic Gyre, re-
ported instances where bacterial biomass equaled
the phytoplankton biomass (Li et al., 1992) or even
exceeded the phytoplankton primary production
(Fuhrman et al., 1989; Cho and Azam, 1990).
In part because of this variability, the dierences
between oceanic regions in microbial loop dynam-
ics and in the fraction of primary production pro-
cessed by heterotrophic bacteria remained unclear
until the discovery of Prochlorococcus cyanobacteria
(Chisholm et al., 1988), which completely changed
the knowledge of the microbial plankton composi-
tion in oligotrophic waters.
Overall, these discoveries stressed the need to
investigate the energy balance in different trophic
systems and the major oligotrophic oceanic prov-
inces. The energy balance can be expressed by the
balance between gross primary production by phy-
toplankton (GPP) and community respiration (CR),
in which bacterial respiration (R) can comprise a
large proportion (50 to 90%) (Rivkin and Legendre,
2001). If GPP>R, the system is in a state of net au-
totrophy and can sustain the export, or sequestra-
tion, of dissolved oxygen, reduced carbon, and the
potential energy that this represents. Otherwise, if
GPP<R, the system is in a state of net heterotrophy
and must import reduced carbon and oxygen to
sustain life, also even suggesting an output of CO2
from parts of the ocean to the atmosphere (Karl,
2007).
Until the end of the 1990s, however, microbial
ecology in the SAO was completely unknown (Figure
4 and Table S3), and most of the studies of organic-
carbon ow through bacterioplankton used empiri-
cal models (Del Giorgio et al., 1997; Del Giorgio and
Cole, 1998). These studies suggested that the rela-
tionship between bacterial grow eciency (BGE) and
BP is variable and that BGE varies systematically with
BP, and the trophic richness of the environment in-
creases from marine regions to estuaries (Cole et al.,
1988; Cho and Azam, 1988).
In attempt to better understand the coupling be-
tween phytoplankton and heterotrophic bacteria and
the growing interest in the carbon cycle in the face of
ocean global changes, in the last two decades, direct
measurements of GPP and R came to be widely used
to derive estimates of net community metabolism in
the oligotrophic open ocean (Serret et al., 2001), includ-
ing the rst metabolic state assessments of the SASG
(Gonzalez et al., 2002; Hoppe et al., 2002; Serret et al.,
2002). These studies sometimes report a prevalence of
heterotrophy (GPP<R) (Serret et al., 2001; Gonzalez et al.,
2002; Hoppe et al., 2002; Duarte et al., 2013), and others a
prevalence of autotrophy (GPP>R) (Williams, 1998; Serret
et al., 2002; Williams et al., 2013, Tilstone et al., 2015).
In turn, some studies conducted along Atlantic
transoceanic transects, have reported alternating
patches between heterotrophic and autotrophic net
community metabolism on both temporal (Arístegui
and Harrison, 2002) and latitudinal scales (González
Figure 4. Cross comparison of Activity Index (AI) on marine ecology research from 1985 (year corresponding
to the rst study in the oligotrophic open ocean) to 2020, between the ve major oligotrophic subtropical
gyres: North Atlantic Gyre, North Pacic Gyre, South Pacic Gyre, Indian Gyre and the South Atlantic Gyre. The
numbers above the bars correspond to AI calculated for SASG.
Microbial ecology of the South Atlantic Gyre
Ocean and Coastal Research 2021, v69:e21027 6
Frazão et al.
et al., 2002; Hoppe et al., 2002), with large net-hetero-
trophic regions. Overall, these studies have revealed
seasonal and geographical patterns, suggesting that
the plankton community structure inuences the net
ecosystem metabolism, thus limiting the predictive
ability of GPP:R relationships. Further investigations
conducted in the Pacic, Atlantic and Arctic oceans
corroborated previous studies, showing that bacte-
rioplankton communities dier among the temper-
ate, subtropical, tropical and polar provinces (Falcón
et al., 2008; Gasol et al., 2009; Westberry et al., 2012).
These studies also suggest that the variability of R,
and not only of primary production, needs to be con-
sidered in estimations of the ocean metabolic status
(Serret et al., 2015).
Despite being intensively investigated, the met-
abolic balance of oligotrophic gyres remains con-
troversial and an active debate about the carbon
balance in oligotrophic pelagic marine ecosystems
is still ongoing (Duarte et al., 2013; Williams et al.,
2013; Tilstone et al., 2015), highlighting the need to
improve knowledge about microbial metabolism in
subtropical oligotrophic gyres.
Most recent approaches based on omics” analy-
ses (metagenomics, metatranscriptomics, meta-
proteomics, metabolomics and metabarcoding)
have provided new insights into the metabolic po-
tential of the oceans and biogeographic patterns
(Morales et al., 2011; Stegen et al., 2013; Aylward et
al., 2015; Lechtenfeld et al., 2015; Logares et al., 2020).
Although these types of analyses do not provide di-
rect information on bacterial production, they are es-
sential to infer microbial community dynamics for the
carbon cycle based on its genetic composition and
metabolism (DeLong et al., 2006). Genomic and post-
genomic analyses, paired with other approaches to
evaluate bacterial production, have rened investiga-
tions of marine microbial ecology and biogeochemi-
cal processes in unprecedented detail. These analy-
ses have also provided important insights to reach
a predictive understanding of shifts of microbial
communities in a changing global ocean, and con-
sequently of potential changes in carbon ow in the
pelagic system (Hutchins and Fu, 2017; Manrique and
Jones, 2017; Allen et al., 2020; Grossart et al., 2020).
In turn, metagenomic analyses, designed to ad-
dress questions related to genetic and biochemical
microbial diversity, have revealed the astounding
diversity and heterogeneity contained in microbial
communities, as well as biogeographic patterns
based on metagenomic sequence similarity pertain-
ing to the temperate Atlantic, tropical Atlantic and
tropical Pacic oceans, including both coastal and
open-ocean sites (Rusch et al., 2007; Falcón et al.,
2008). In the last 15 years, important contributions in
this eld have been provided by ocean expeditions
such as the Global Ocean Sampling (GOS) (Rusch et
al., 2007), the Malaspina Circumnavigation (Duarte
et al., 2015) and the Tara Oceans Project (Sunagawa
et al., 2020), which also made it possible to address
the question of how microbial communities adjust to
global environmental variations on a planetary scale.
Most recent investigations are also focusing on
advancing the understanding of how ocean changes
such as warming and acidication may aect the bio-
logical carbon pump (BCP) and the microbial carbon
pump (MCP), as well as the potential transition from
dominance of the BCP to the MCP in oligotrophic
oceans (Zhang et al., 2017). BCP depends on photo-
synthetic xation of CO2 and subsequent carbon ex-
port, driven mainly by sinking of particulate organic
carbon. The MCP is a component of the BCP concept,
used to describe the microbial production of refrac-
tory DOM (RDOM), which can be stored for millennia
in the deep sea, rather than being respired as dis-
solved inorganic carbon and returned to the atmo-
sphere (Jiao et al., 2010; Jiao and Azam, 2011). Both
processes have signicant eects on the air-sea CO2
uxes on century time scales (IPCC, 2013) and are cru-
cial to ocean carbon ow and climate control.
CURReNT kNOwleDge Of MICRObIAl eCOlOgy IN The
sOUTh ATlANTIC sUbTROpICAl gyRe
Data assessment
To assess current knowledge of microbial ecol-
ogy in the South Atlantic Subtropical Gyre, we per-
formed a new screening from the results of the rst
step of our search (i.e. methodological approaches)
on the Web of Science portal (www.webofscience.
com). Through a search of keywords in the title, and
when this was not sucient, by reading the publica-
tion abstract, or yet, methodologies, we selected only
studies conducted in oligotrophic areas of the SAO:
the South Atlantic Subtropical Gyre (SASG) and the
Southwestern Atlantic Ocean (SWAO) (Figure 5).
Microbial ecology of the South Atlantic Gyre
Ocean and Coastal Research 2021, v69:e21027 7
Frazão et al.
Figure 5. Schematic representation of the main steps of our searching strategy for publications on marine microbial
ecology on SASG, through the Web of Science Portal. Black diamonds represent the total number of publications.
Blue diamonds represent the total number of citations for the ve major subtropical gyres: North Atlantic Gyre, North
Pacic Gyre, South Pacic Gyre, Indian Gyre and the South Atlantic Gyre, from 1974 to 2020.
Our search involving microbial ecology in this
region resulted in 38 studies, of which 32 were con-
ducted in the open ocean area of the SASG and six
in the southwestern Atlantic, comprising the South
Brazilian Bight (SBB). This total number suggests that
microbial ecology remains poorly studied in the SAO,
compared to other oligotrophic ocean basins.
Considering that the simple numerical counting
of the absolute number of selected articles can lead
to erroneous conclusions (Kumari, 2006), we quanti-
ed these contributions by calculating an Activity
Index (AI). Initially suggested by Frame (1977) and
used in several scientometric assessments (Brusoni
and Geuna, 2003; Thomaidis et al., 2000; Kumari,
2006), AI normalizes the publication prole, i.e. one
region in relation to the others.
For a cross-comparison between the ve major
subtropical gyres (North Atlantic Gyre, North Pacic
Gyre, South Pacic Gyre, Indian Ocean Gyre and the
South Atlantic Gyre), we calculate the AI as follows:
Activity Index (AI) of given gyre g:
{Number of Publications in marine microbial ecology
(MME) in gyre g in year y / Total number of publications
for all years for that gyre} / {Total MME in all gyres output
in year y / Total MME in all gyres output for all years}.
AI = 1 indicates that the number of research stud-
ies on the gyre is relatively equal to the other gyres.
AI > 1 indicates that research eorts on the gyre
are higher than average compared to the others gyres
AI < 1 indicates lower research eorts on the gyre
compared to the global output.
Despite the absolute number of publications
pointing to a greater research eort in the North
Atlantic Gyre and North Pacic Gyre (Table S3), the
calculated AI showed a great eort in the SASG in
some periods over the last twenty years in compari-
son with the other gyres in the southern hemisphere,
mainly between 2015 and 2017 (Figure 4).
In addition, we present the main information
from these 38 studies in the SASG and a database
of available data on microbial parameters and envi-
ronmental variables (Table S2). We also compiled the
sampling stations where each study was conducted,
in an attempt to provide an overview of the studied
area in the oligotrophic SAO (Figure 6).
statistical analyses
In order to explore general patterns of micro-
bial parameters in the SASG, initially we applied
multivariate analysis techniques to the current da-
ta (log-transformed) available for those listed by
sampling station (Table S2). Principal component
analysis (PCA) was applied for microbial plankton
abundance (heterotrophic and autotrophic bac-
teria, eukaryotic picoplankton) and environmen-
tal variables (temperature, salinity and inorganic
nutrients), to investigate the main environmental
drivers of microbial abundance.
Microbial ecology of the South Atlantic Gyre
Ocean and Coastal Research 2021, v69:e21027 8
Frazão et al.
Figure 6. Sampling stations from studies conducted in the
SASG and SWAO, extracted from the 38 publications resulting
from our review. (A) Studies involving bacterial abundance by
ow cytometry/epiuorescence microscopy and/or bacterial
production by radioisotopic methods, and/or metabolic state
by O2 method; green triangles indicate studies conducted in the
epipelagic zone, red squares indicate studies conducted in the
deep ocean. (B) Studies involving metagenomic or metaproteomic
analyses (taxonomic or functional composition); green circles
indicate metagenomic analyses in the epipelagic zone, blue
triangles indicate metaproteomic analyses in the epipelagic zone,
and red squares indicate metagenomic analyses in the deep ocean.
Additionally, we performed descriptive statistics
using box plots and ANOVA tests to visualize and an-
alyze dierences in microbial abundances between
regions, seasons and depths. Pearson´s correlations
and simple linear regressions were also applied to
measure the linear dependences between normal-
ized biotic and abiotic data.
For all analyses, the dataset was classied accord-
ing to the sampling location, SWAO or SASG (western
and eastern boundaries of the SASG, or central gyre)
and its respective layer (euphotic zone, depth maxi-
mum chlorophyll (DCM), or mesopelagic zone).
The PCA analyses were performed using the
FactoMinerR package available in R statistical soft-
ware version 3.6.3 (Lê et al., 2008). The box plots,
followed by an ANOVA test, as well as the Pearson´s
correlation coecient and the linear regressions,
were performed using the software PAST version 4.02
(Hammer et al., 2001).
CURReNT kNOwleDge IN The OpeN OCeAN Of sOUTh
ATlANTIC sUbTROpICAl gyRe (sAsg)
The pioneer studies concerning microbial ecol-
ogy in the open ocean of the SASG date only from
the last two decades (Figure 4 and Table S3). The rst
investigations in this region were based on a series of
cruises of the Atlantic Meridional Transect (AMT) pro-
gram which had as one of its main goals to advance
understanding of the picoplankton community
structure and function over a wide latitudinal range.
Focusing on the role of the oceans in the global car-
bon cycle, these early studies compared the micro-
bial composition (Zubkov et al., 1998; 2000a; 2000c)
and heterotrophic bacterial production (Zubkov et
al., 2000b) in the North and South Atlantic over a
meridional transect from 50°N to 50°S. The composi-
tion of the picoplankton community, including het-
erotrophic bacteria, eukaryotic picophytoplankton,
Synechococcus and Prochlorococcus, indicated that
this area could be grouped into ve large regions,
presently called the North Atlantic Drift Province
(NADR), North Atlantic Tropical Gyre (NATL), Western
Tropical Atlantic (WTRA), South Atlantic Subtropical
Gyre (SASG) and the South Subtropical Convergence
(SSTC). These results also indicated that heterotro-
phic bacterial production is lowest in the North and
South Atlantic gyres, tending to be highest where the
phototrophic biomass is highest.
Over the same transect (AMT), González et al.
(2002) investigated microbial metabolism using di-
rect measurements of GPP:R. This study also showed
that the region of the South Atlantic Gyre is less pro-
ductive than the other Atlantic provinces, tending
to a net heterotrophic balance (GPP<R). Hoppe et
al. (2002) also investigated the net community me-
tabolism of the South Atlantic Subtropical Gyre in
an expanded meridional transect, from 53°N to 65°S.
Their results were consistent with previous studies
in this region, showing that the South Atlantic was
Microbial ecology of the South Atlantic Gyre
Ocean and Coastal Research 2021, v69:e21027 9
Frazão et al.
in net heterotrophic balance. In contrast, the study
conducted by Serret et al. (2002) in the central SASG
showed a prevalence of net autotrophy in this region
(GPP>R), suggesting the existence of dierent tro-
phic dynamics in similarly unproductive planktonic
communities. Both studies also found that the ratio
between BP and primary production was closely re-
lated to the meridional prole of water temperature,
with a predominance of net heterotrophy in the
warm oligotrophic regions.
Later studies also focused on the microbial me-
tabolism underlined the inuence of the regional and
temporal variability of nutrient inputs on biomass
and heterotrophic bacterial production (Hoppe et al.,
2006; Vázquez-Domínguez et al., 2008; Zubkov et al.,
2008; Gasol et al., 2009; Gist et al., 2009, Otero-Ferrer
et al., 2018), reinforcing a global dependence of bac-
terial activity and production on the nutrient supply.
Focusing on the rst predictions of organic mat-
ter inputs of atmospheric origin into the oceans
(Dentener 2006; Duce 2008), two relevant studies
involving microcosm experiments were conducted
over a wide latitudinal transect in the Atlantic Ocean,
including the central SASG (26°N to 29° S). Martínez-
García et al. (2010) in an attempt to determine gen-
eral patterns in the connection between the type
of organic matter input, the initial biotic and abiotic
conditions and the interactions between microbial
compartments, showed that bacterioplankton re-
sponses were much higher than phytoplankton re-
sponses when both inorganic and organic nutrients
were supplied, thus potentially driving the microbial
community towards heterotrophy. Teira et al. (2010)
investigating changes in the relative abundance of
the bacterioplankton community composition at the
level of major taxonomic groups observed that dis-
tinct groups responded dierently to nutrient addi-
tions: SAR11 and Bacteroidetes responded negative-
ly to organic and mixed additions, while Roseobacter
spp. and Gammaproteobacteria responded posi-
tively. A clear increasing gradient from north to south
in the magnitude of the Gammaproteobacteria re-
sponse to organic inputs (containing carbon and
nitrogen) suggested a strong link between bacterial
community composition and carbon cycling in the
oligotrophic ocean.
Other studies focusing on bacterial metabolic ac-
tivities have assigned temperature as the main driver
of bacterial production. Hill et al. (2011) suggested
that bacterial activity is a sensitive marker of gyre
boundaries and distinct water masses. Mazuecos et
al. (2015) through derived PGE indicated a strong
correlation between R and PGE across a temperature
gradient, suggesting that temperature variability in
the mesopelagic zone plays a signicant role in the
remineralization of organic matter.
Evans et al. (2015) based on experimental results
of light-enhanced uptake of methionine, leucine and
ATP by Prochlorococcus and SAR11, provided new
evidence of bacterial metabolism, indicating that
photoheterotrophy is characteristic of dominant bac-
terioplankton populations in the global oligotrophic
ocean and a widespread biological process in the
SASG.
Still focusing on the metabolic state of subtropi-
cal oligotrophic gyres, Serret et al. (2015) and Tilstone
et al. (2015) provided important contributions to the
discussion that is still ongoing. To test the assump-
tion that no regional dierences exist in either the
P:R relationship or the metabolic balance through
the oligotrophic ocean, Serret et al. (2015) compiled
vertical proles of the in-vitro GPP, R and net commu-
nity production (NCP) measurements made during
the Atlantic Meridional Transect (AMT) cruises from
2000 through 2012. Based on the dierences in both
GPP and R, the authors demonstrated the existence
of systematic dierences in the metabolic state of the
oligotrophic North and South Atlantic gyres, reinforc-
ing the previously suggested theory that the oligo-
trophic ocean is neither auto- nor heterotrophic, but
functionally diverse. With the main goal of deriving
accurate estimates of net community production,
Tilstone et al. (2015) compared a number of empiri-
cal approaches using primary production data from
satellites with in-vitro measurements of changes in
dissolved O2 concentrations in the North and South
Atlantic Ocean. Their results showed that the South
Atlantic Subtropical Gyre uctuated from being net
autotrophic in austral spring-summer, to net hetero-
trophic in austral autumn-winter, indicating that re-
cent decadal trends suggest that the SASG is becom-
ing a more important source of CO2.
Finally, in terms of deriving the metabolic state
of SASG, García-Martín et al. (2017) conducted direct
measurements of bacterial respiration along north
to south transects (50.45°N to 44.33°S), including the
Microbial ecology of the South Atlantic Gyre
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Frazão et al.
dissolved O2 concentration. Results from this study
showed a signicantly higher cell-specic bacterial
respiration in the temperate and upwelling regions
compared with oligotrophic gyres, including the
SASG, which suggests that bacterial carbon turnover
is slower in this province. The study also showed that
the bacterial contribution to depth-integrated com-
munity respiration varied widely within provinces (4–
77%), suggesting that the proportion of total com-
munity respiration attributable to bacteria is similar
in the dierent oceanographic regions studied.
Concerning –‘omics analyses, the rst studies us-
ing genomic approaches in the SASG have agreed
with these previous studies, also showing dierent
patterns of latitudinal distribution of the taxonomic
composition and diversity of the bacterial communi-
ty. Schattenhofer et al. (2009) and Morris et al. (2012)
showed that SAR11 bacterioplankters are less abun-
dant in the South Atlantic than in the North Atlantic,
and that the biomass of Prochlorococcus reached its
peak in this region. Morris et al. (2010), conducted
the rst and unique metaproteomic study in the
SASG and indicated that the microbial community
structure also shifted along the nutrient concentra-
tion gradients, from the open ocean to the coast.
Swan et al. (2014) were the rst to investigate the ge-
nomic and metabolic diversity of Thaumarchaeota,
one of the most abundant and cosmopolitan chemo-
autotrophs within the global dark ocean. This study,
however, included only one sampling station in the
mesopelagic zone of the SASG.
Important contributions for current knowledge
of microbial structure, diversity, function, activ-
ity and biogeographical patterns in the SASG were
provided by the Tara Oceans Project, Malaspina
Circumnavigation Expedition and the GEOTRACES
cruises. Metagenomic data from these global expedi-
tions are available from Sunagawa et al. (2015), Tully
et al. (2017), Biller et al. (2018) and Sanz- Saéz et al.
(2020).
Overall, these studies assessed patterns of diver-
sity and marine stratifying factors of the microbial
community composition from dierent depths, gen-
erating unprecedented amounts of environmental
sequencing data and making it possible to address
the question of how microbial communities respond
to global environmental variations. The Malaspina
Expedition, in turn, provided an unprecedented as-
sessment of the state of the dark ocean, allowing for
the rst global assessment of bacterial abundance
in mesopelagic and bathypelagic waters of the main
ocean basins. Data on the bacterial abundance in
the SASG deep ocean are available from Pernice et
al. (2015). Tully et al. (2017) reconstructed microbial
genomes from these metagenomics samples, pre-
senting 360 additional draft genomes from the SAO
samples for Bacteria and Archaea.
In light of the need to understand the current
and future conguration of marine microbes in the
global ocean, recent studies examined the ecological
mechanisms that shape these microorganisms in sur-
face waters on a planetary scale. From samples ob-
tained from the Tara Ocean Project and the Malaspina
Expedition, Logares et al. (2020) identied patterns
using amplicon sequencing data, suggesting that the
surface water picoplankton may not show a single re-
sponse to global change, and that perhaps prokary-
otes will display more pronounced changes in their
community structure as a response to temperature
increase than picoeukaryotes.
Finally, the most recent study on SASG analyzed
a collection of 31 metagenomes including the epipe-
lagic, mesopelagic and bathypelagic zones (Coutinho
et al., 2021). By revealing that many of these ge-
nomes are derived from poorly characterized taxa of
Bacteria and Archaea, these results reinforce the less-
er attention that the SASG microbiome has received
compared to other regions of the global ocean.
CURReNT kNOwleDge Of The sOUThwesT ATlANTIC
OCeAN (swAO)
Microbial communities in the Southwest Atlantic
Ocean (SWAO) o Brazil are beginning to be inves-
tigated, but studies conducted in the southwestern
portion of the SAO, especially on the inner shelf of
the South Brazilian Bight (SBB), have also provided
evidence of the dependence of bacterial production
on the nutrient supply, the coupling of heterotrophic
bacteria and primary producers, as well as the tem-
poral variability in the metabolic state of open oligo-
trophic waters.
The SWAO is one of the most oligotrophic ar-
eas in the entire ocean (Alves Junior et al., 2015);
the waters on the Brazilian continental shelf, which
Microbial ecology of the South Atlantic Gyre
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Frazão et al.
are predominantly autotrophic, are fertilized during
spring and summer by the onshore intrusion of the
oceanic South Atlantic Central Water (SACW), a cold
and nutrient-rich water mass (Castro et al., 2006).
The rst study concerning bacterial dynamics in
the SWAO (Andrade et al., 2004) was conducted over
a broad area of the Atlantic Ocean, from São Tomé
Cape (ST Cape; 22°S, 41°W) to the Salvador coast
(13°S, 38°W), and o the Brazilian oceanic islands
Trindade and Martim Vaz (20°S, 29°W). The authors
conducted a preliminary characterization of bacte-
rioplankton in this region and evaluated the hetero-
trophic bacterial abundance and production over
this large spatial scale. Their results addressed the re-
lationship of bacteria distribution and activity to up-
welling phenomena in this area of the southwestern
Atlantic Ocean.
In the same region, Andrade et al. (2007) investi-
gated the distribution pattern of the high nucleic ac-
id content (HNA) and low nucleic acid content (LNA)
bacteria, and their relationship to physical and chem-
ical features. Their results showed the distribution of
these groups in two dierent oceanic provinces, from
coastal waters to the open ocean: HNA bacteria were
dominant in warmer waters with riverine nutrient
inputs, and LNA bacteria were the dominant cells in
regions with higher nitrate levels.
To assess the distribution of pico- and nanoplank-
ton communities in dierent water masses on the in-
ner shelf of the South Brazilian Bight (SBB), Ribeiro et
al. (2016a; 2016b) determined the abundance of het-
erotrophic bacteria, Prochlorococcus, Synechococcus
and autotrophic pico- and nanoeukaryotes along
three transects extending from 23°S to 31°S and
39°W to 49°W. The results obtained from this study
agree with observations in other marine areas, where
Synechococcus and autotrophic eukaryotes domi-
nate the mesotrophic waters, while Prochlorococcus
dominates in oligotrophic areas. Using the same ap-
proach, Bergo et al. (2017) assessed the inuence of a
summer intrusion of the South Atlantic Central Water
(SACW) on the spatial and vertical dynamics of plank-
ton abundance and carbon biomass across environ-
mental gradients. Regarding the importance of each
group to carbon biomass partitioning, the authors
showed that the dominance of heterotrophic bac-
teria is governed by upwelling conditions, while the
relative contribution of each phytoplankton group
is more evenly distributed when the SACW is not as
inuential.
Finally, we highlight the rst metagenomic study
conducted in the SWAO, which covered the Abrolhos
Bank and the Campos Basin (from -08° to -23° lati-
tude), both in the southwestern Atlantic (Alves
Junior et al., 2015). This study was the rst attempt,
and unique until now, to characterize the taxonomic
and functional community diversity along the depth
continuum and dierent water masses in the SWAO
and to compare this diversity with the microbial
community diversity of the global ocean. The results
showed that the SWAO has a signicant proportion
of endemic genetic diversity and a unique microbial
signature. SWAO microbial communities share genes
with the global ocean in at least 70 cellular functions;
however, more than a third of reported genome se-
quences comprise a unique gene pool in the global
ocean. This interesting study suggests that the SWAO
is maybe a hotspot of microbial diversity.
DIsCUssION
Despite the facilities provided by the method
used in our search for scientic articles, it is possible
that some restrictions in this database have resulted
in an underestimation of our results concerning stud-
ies on marine microbial ecology. Thus, we must con-
sider our result (n=758) as a rough estimate of the
total scientic publications over these years, which
in turn allowed us to address the methodological
trends and the main conceptual advances in this eld
over the last ve decades, regarding oligotrophic pe-
lagic ecosystems.
These same facilities allowed us to easily access
publications that have at least one sampling station
in the region of interest (SASG/SWAO), and compile
the number of publications in each of the ve main
subtropical gyres used to calculate the AI (Figure 5).
Despite the last two decades of experimental
and eld observations, four central issues have ham-
pered eorts to eectively improve knowledge of the
mechanisms that shape microbiological and biogeo-
chemical processes in this region: 1) the controversy
over its metabolic balance/state, 2) the main drivers
of biogeographic patterns in the microbial commu-
nity composition, 3) lack of knowledge about taxo-
nomic composition, 4) spatial and temporal unders-
ampling, especially in deep layers.
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Frazão et al.
Since the balance between net autotrophic and
heterotrophic production by direct measures of GPP
and R was the most investigated topic in the SASG,
the spatial distribution and temporal variability of the
sampling, as well as dierences due to the use of dif-
ferent methods, may explain the lack of agreement
on its metabolic state.
Concerning the dierences in spatial distribu-
tion, the rst investigations conducted in the SASG
already suggested the existence of dierent trophic
dynamics within the gyre. Gonzales et al. (2002) and
Hoppe et al. (2002) investigating the western bound-
ary of the SASG showed a net heterotrophic balance
(R >GPP), while Serret et al. (2002) investigating the
central SASG showed a prevalence of net autotrophy
(GPP>R). A series of other studies have also reported
dierences in the metabolic state of the SASG, in-
cluding seasonal trends (Vasquez-Dominguez et al.,
2008; Zubkov et al., 2008; Gasol et al., 2009; Serret et
al., 2015; Tilstone et al., 2015). Overall, these studies
reinforce the existence of regional and temporal vari-
ability in the trophic dynamics of the gyre, suggest-
ing that the inuence of nutrient inputs may be more
important than temperature in the regulation of bac-
terial growth characteristics on a large spatial scale.
Later studies focusing on bacterial metabolic ac-
tivities, however, attributed temperature as the main
driver of biomass and heterotrophic bacterial produc-
tion (Hill et al., 2011; Mazuecos et al., 2015, Logares et
al., 2020). The geographic pattern of the net commu-
nity metabolism was also attributed to the functional
diversity of the SASG pelagic ecosystem, highlighting
to the relative importance of local vs. allochthonous
sources of organic matter. Since the responses of het-
erotrophs and autotrophs to nutrient inputs are dif-
ferent (Martínez-García et al., 2010; Teira et al., 2010),
it is suggested that dierent processes control bacte-
rial dynamics in oligotrophic waters.
Over the last ve years, the advancement of
metagenomic studies in the SASG, as well access to
the taxonomic and genomic content of global ocean
microbial communities (Sunagawa et al., 2015; Tully
et al., 2017; Biller et al., 2018; Logares et al., 2020;
Sans-Saéz et al., 2020; Coutinho et al., 2021), have
provided new evidence of the diversity and function-
al patterns of this region. This new evidence has also
emerged with new questions, suggesting that the
geographic pattern of net community metabolism
may be related to the functional diversity of each
ocean basin.
This variability between regions and years is expected
due to dierences in the physicochemical characteristics
and microbial community composition. In an attempt
to nd general patterns in the SASG that would illumi-
nate some of these questions, we conducted statistical
analysis using microbial abundance and environmental
parameters of data currently available (Table S2). These
analyses allowed us to explore some of these issues and
provide support to answer the following questions: Are
there any geographic, seasonal and/or depth patterns
in the abundance and diversity of microbial plankton
subgroups in the oligotrophic SAO (SASG/SWAO)? Are
there dierent patterns of these variables within the gyre
(SASG)? What are the main environmental drivers shap-
ing these microbial parameters in these regions?
The rst PCA analysis (n= 334) applied to both
regions of oligotrophic SAO (SASG/SWAO) indicated
that the rst two components are sucient to ex-
plain 90.6% of the total variance of microbial and
environmental variables (Figure 7A). PC1 explained
57.9% of the data variability, while PC2 explained
32.7% of the variability. The highest contributions
to PC1 were eukaryotic picoplankton, PO4 and NO2,
while the highest contributions to PC2 were temper-
ature, heterotrophic bacteria and NO3. These results
showed a strong relationship between heterotrophic
bacterial abundance and temperature, and between
autotrophic picoplankton and NO3 concentration
in both regions. The biplot graph also showed the
grouping of samples according to the spatial (SASG
vs. SWAO) and vertical distribution. For samples from
mesopelagic zones, it is possible to notice similarities
for both regions. For the euphotic zone of the SWAO,
no spatial distribution pattern was observed.
To further explore spatial patterns in the SASG,
we applied an additional PCA (n = 170) including
only the dierent areas of the gyre (central (SASG),
western boundary (WB-SASG) and eastern bound-
ary (EB-SASG)). For this PCA analysis (Figure 7B), the
two components explained 99% of the total variance.
PC1 explained 76% of the variability, while PC2 ex-
plained 23%. Heterotrophic bacteria, salinity and PO4
were the major contributors to PC1, while nitrate and
eukaryotic picoplankton were the main contributors
to PC2. This biplot indicated a clear vertical and geo-
graphic pattern, showing that in the euphotic zone
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Frazão et al.
of the western boundary of the SASG, autotrophic
picoplankton and NO3 are positively correlated, while
heterotrophic bacteria are more connected with the
temperature in the euphotic zone of the central and
western boundary of the SASG.
The analysis of the box plots, followed by verica-
tion of the result of the ANOVA test, both performed
to investigate the dierences in microbial abundance
between regions, seasons and depths, indicated sig-
nicantly higher abundance (p-value<0.001) of het-
erotrophic bacteria in the SWAO region compared
to the SASG (Figure 8A), but lower abundance of
autotrophic bacteria when compared to the western
boundary of the SASG (WB-SASG) (Figure 8D). When
contrasting microbial abundance between seasons,
heterotrophic bacteria showed a more homoge-
neous distribution, whereas autotrophic bacteria
were signicantly (p-value<0.001) higher in autumn
than in spring or summer (Figure 8E). Interestingly,
the abundance of eukaryotic picophytoplankton did
not show signicant dierences between seasons or
between study regions (Figure 8G and H). Regarding
depth, signicant dierences (p-value<0.01) in micro-
bial abundance were found along the water column,
being signicantly lower in the mesopelagic zones
than in the DCM and euphotic zones (Figure 8C, F
and I).
In addition, the analysis of Pearson’s correlation
coecients (r) (Table 1) showed a strong positive
correlation between temperature and heterotrophic
Figure 7. Biplots of the principal component analysis (PCA) of microbial abundances from ow cytometry
(heterotrophic bacteria (HeBac), autrotrophic bacteria (AuBac), eukaryotic picoplankton (EuPico)) and environmental
parameters (temperature (T), Salinity (Sal), Phosphate (PO4), Nitrate (NO3), Nitrite (NO2) and Silicate (Si)) for the
oligotrophic regions of SAO. Circles represent the data in the euphotic zone, squares represent the samples from
the depth of chlorophyll maximum (DCM), and triangles represent the samples in the mesopelagic zone. The size of
the lines indicates the contribution of the components. Dierent colors represent the dierent regions: (lilac) central
SASG, (red) eastern boundary of the SASG (EB-SASG), (blue) western boundary of the SASG (WB-SASG), (orange) the
oligotrophic SWAO. (A) PCA applied for SASG and SWAO. (B) PCA applied only for the dierent regions in the SASG.
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Frazão et al.
Table 1. Pearson's correlation coefficient (r) between microbial abundances from flow cytometry (heterotrophic bacteria (HeBac),
autrotrophic bacteria (AuBac), eukaryotic picoplankton (EuPico)) and environmental parameters (Temperature (T), Salinit y (Sal), Nitrate
(NO3), Nitrite (NO2), Phosphate (PO4), Silicate (Si), and Chlorophyll fluorescence (Flu)).
bacterial abundance (r = 0.71) and a moderate posi-
tive correlation with the abundance of autotrophic
bacteria (r = 0.51), which were corroborated by linear
regressions (Figure 9). Depth was negatively correlat-
ed with heterotrophic (r = -0.65) and autotrophic (r =
-0.52) bacterial abundance, which was also revealed
Figure 8. Box plots of microbial abundance data from ow cytometry (Log10 abundance): (A-C) Heterotrophic
bacteria, (D-F) Autotrophic bacteria, (G-I) Eukaryotic picophytoplankton. Data are grouped according to study
region (central SASG (SASG), eastern boundary of the SASG (EB-SASG), western boundary of the SASG (WB-
SASG), and SWAO), season (spring, summer, autumn and winter) and pelagic zone (DCM, mesopelagic and
euphotic zone). The p-values obtained in the ANOVA tests are indicated in the graphs, for each data group.
HeBac AuBac EuPico Depth TSal NO3NO2PO4Si Flu
HeBac 1
AuBac 0.512 1
EuPico 0.534 0.466 1
Depth -0.654 -0.518 -0.197 1
T0.714 0.511 0.190 -0.646 1
Sal 0.210 0.121 -0.050 -0.264 0.634 1
NO3-0.635 -0.666 -0.232 0.661 -0.787 -0.486 1
NO20.291 -0.082 0.204 -0.036 0.185 0.017 0.110 1
PO4-0.356 -0.336 -0.217 0.457 -0.604 -0.528 0.629 0.066 1
Si -0.295 -0.117 0.193 0.414 -0.643 -0.660 0.598 -0.048 0.800 1
Flu 0.255 0.258 0.569 0.168 0.017 0.017 -0.070 0.347 -0.068 0.126 1
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Frazão et al.
Figure 9. Linear regressions between microbial abundance data from ow cytometry and environmental parameters (temperature (T),
nutrients (NO3 and PO4) and chlorophyll uorescence (Flu)): (A-D) Heterotrophic bacteria, (E-H) Autotrophic bacteria, and (I-L) Eukaryotic
picophytoplankton.
by box plot analyses. Nutrient concentrations, mainly
NO3 and PO4, also showed negative correlations with
bacterial abundance. This trend was especially ob-
served for autotrophic bacteria versus nitrate (Figure
9F). The abundance of eukaryotic picophytoplankton
showed a positive correlation with chlorophyll uo-
rescence (r = 0.57), which was corroborated by the
linear regression (Figure 9L).
Overall, these analyses support biogeographic
patterns of microbial communities in dierent areas
of oligotrophic SAO (SASG vs. SWAO), between two
areas within the gyre itself (i.e., marginal vs. central),
as well as dierences between seasons and depths.
They also indicate the relative importance of dier-
ent local vs. allochthonous sources of organic matter
on microbial structure, suggesting that SASG is pre-
dominantly autotrophic, acting as CO2 sink.
At an ocean-wide scale, dierent environmental
conditions regulate the growth characteristics of pi-
coplankton. While the growth of autotrophic bacte-
ria and eukaryotic picophytoplankton are supported
by nutrients, the growth of heterotrophic bacteria
is partially supported by organic compounds pro-
duced by phytoplankton cells and remineralization of
inorganic nutrients (Azam et al., 1983). Thus, due the
coupling between phytoplankton and heterotrophic
bacteria, changes in the microbial community are ex-
pected along a nutrient gradient and under dierent
environmental conditions. This explains the highest
abundance of heterotrophic bacteria in SWAO com-
pared to SASG, and the highest abundance of auto-
trophic bacteria in the SASG.
The growth of heterotrophic bacteria in SWAO
benets from increased organic matter derived from
phytoplankton communities and allochthonous
sources (Susini-Ribeiro et al., 2013, Brandini et al.,
2014). The growth of autotrophic bacteria in WB-SASG
is inuenced by the seasonal (spring-summer) intru-
sion of the nutrient-rich South Atlantic Central Water
(SACW) along the adjacent continental shelf of SWAO
(Castro et al., 2006, Ribeiro 2016b, Bergo et al., 2017),
which promotes fertilization of the euphotic layer
through a shift from regenerated to new production
(Metzler et al., 1997). In the most central SASG and
eastern boundary, the highest abundance of autotro-
phic bacteria is supported by Prochlorococcus, which
dominate in more oligotrophic areas (Partensky et al.,
1999). Regarding the dierences between seasons,
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Frazão et al.
the lower abundance of autotrophic bacteria in
spring and summer can also be explained by the up-
welling phenomena on the SWAO continental shelf
(Ribeiro et al., 2016b, Bergo et al., 2017), which favors
the growth of larger phytoplankton cells. With re-
spect to eukaryotic picophytoplankton, their ability
to move in the water column in response to dierent
light and nutrient gradients to improve their optimal
growth conditions (Raven, 1998) may explain their
positive correlation with chlorophyll uorescence.
Since photosynthesis (GPP) and respiration (BP)
mediate the exchange of CO2 between the oceans
and atmosphere (Duarte et al., 2013, Tilstone et al.,
2015), this strong link between microbial plankton
communities and environmental conditions may
provide indication of their role in the carbon cycling
in the oligotrophic ocean, and therefore be appropri-
ate to monitor the eect of possible changes in these
conditions at the microbial level (Hoppe, 2006). Thus,
considering that temperature seems to aect more
prokaryotic assemblages than picoeukaryotes, and
that prokaryotes would present more pronounced
changes in their community structure in response to
temperature increase on a planetary scale (Logares,
2020), the need for improvements is clear for provid-
ing data in open ocean basins and poorly studied
subtropical oligotrophic gyres, such as the SASG.
Previous studies also corroborate these state-
ments, indicating shifts in the structure and diver-
sity of microbial metabolism induced by the sea
surface temperature warming and ocean acidica-
tion (Sarmento et al., 2010; Morán et al., 2015; Huete-
Stauer et al., 2016, Louca et al., 2016). Experimental
studies using microcosms have also revealed the dif-
ferent responses of food web components to warm-
ing, through changes in biomass, production, respira-
tion, and lower growth eciency (Hoppe et al., 2008;
Wohlers et al., 2009; Sarmento et al., 2010; Lara et al.,
2013). Reductions in bacterial size, through genome
sizes, have also proved to be a short-term response
to increasing temperature in experimental incuba-
tions (Morán et al., 2015; Huete-Stauer et al., 2016).
Moreover, the composition of bacterioplankton com-
munity changed consistently in response to elevat-
ed CO2 at the ultraoligotrophic center of the South
Pacic Gyre (Allen et al., 2020).
In view of the direct and indirect evidence
that indicate changes in tropical and subtropical
oligotrophic gyres (Hill et al., 2011; Hu et al., 2017;
Zhang et al., 2017), a shift in the balance between
autotrophic production and heterotrophic con-
sumption of organic matter is expected. A commu-
nity dominated by smaller cells, mainly heterotrophic
bacteria, would favor respiration of carbon in the
microbial loop and reduction of the rate of carbon
sequestration. The consequences of these changes
for ocean ecosystems can be summarized as a po-
tential reduction in the transfer of organic matter to
higher trophic levels, bacterial losses to their grazers
(Wohlers et al., 2009) and weakening of the biologi-
cal and microbial carbon pump, with a positive feed-
back to the rising atmospheric CO2 (Evans et al., 2011;
Morán et al., 2015; Zhang et al., 2017) and potential
changes in carbon ow in the pelagic system.
All of these issues support the need to conduct
large-scale cruises and long-term monitoring pro-
grams across the SASG, in an attempt to integrate
data on bacterial production, primary production,
microbial abundance, taxonomic and genetic diver-
sity. In line with the debate over to whether the oligo-
trophic ocean acts as a CO2 sink or CO2 source to the
atmosphere, eorts including empirical, theoretical
and modeling approaches would help provide data
to eectively improve knowledge about the SASG
and support more accurate predictions in a changing
global ocean.
CONClUsIONs
In light of the exponential rate of progress in ma-
rine microbial ecology in the last few decades, our
attempt to address the state of the art on the South
Atlantic Subtropical Gyre encouraged us to also ex-
plore the dynamics of conceptual and methodologi-
cal advances related to carbon ows and the role of
oligotrophic gyres in the global biogeochemical cy-
cles. In this context, the production of a timeline and
compilation of publications in a historical perspec-
tive allowed us to summarize the main conceptual
and methodological milestones that led to the cur-
rent high level of understanding of the key oceanic
processes with regard to microbial communities and
the biological carbon pump. Furthermore, our over-
view of microbial ecology in oligotrophic open ocean
basins allowed us to reinforce that better knowledge
of subtropical oligotrophic gyres is a central task to
determine the magnitude and variability of carbon
Microbial ecology of the South Atlantic Gyre
Ocean and Coastal Research 2021, v69:e21027 17
Frazão et al.
exported from the surface to the deep ocean, as well
as the exchange CO2 between the atmosphere and
the ocean.
In turn, our compilation of publications on marine
microbial ecology in SASG helped to highlight that the
oligotrophic SAO is still among the least known oceanic
provinces. Despite growing research eorts in this re-
gion over the past two decades, the lack of knowledge
about the metabolic state, the main drivers of biogeo-
graphic patterns and taxonomic composition, together
with undersampling, have hampered eorts to eec-
tively improve knowledge of this region.
Ultimately, our metadata analysis helped reveal
biogeographic patterns of microbial communities
in dierent areas of oligotrophic SAO, highlighting
the relative importance of dierent local vs. alloch-
thonous sources of organic matter for the coupling
between phytoplankton and heterotrophic bacteria
in this region, suggesting that SASG is predominantly
autotrophic, acting as a CO2 sink.
Since previous studies have pointed to tempera-
ture as a key variable for shaping microbial structure
in open ocean basins, current evidence of climate
change and ocean warming from the last IPCC re-
ports challenges the idea that a shift in the balance
between autotrophic production and heterotrophic
consumption in SASG would favor a positive feed-
back for increasing atmospheric CO2.
Therefore, research eorts concerning marine mi-
crobial ecology in open ocean basins and subtropical
oligotrophic gyres have assumed new importance
in predicting the implications of global change for
the microbial plankton community, carbon ow in
the pelagic system, and CO2 exchanges between the
ocean and atmosphere.
ACkNOwleDgMeNTs
This paper was written as a result of a gradu-
ate course (Marine Plankton Secondary Production;
Oceanographic Institute, University of São Paulo).
LRF, SBP, LSM, GMV and CG thank to CNPq (National
Council for Scientic and Technological Development)
and CAPES (Coordination for the Improvement of
Higher Education Personnel - Brazil) for their Master
and Doctorate fellowships. RML is a CNPq fellow
(310642/2017-5). The authors thank Janet Reid for the
English review, as well as the anonymous reviewers for
their careful reading of our manuscript and their many
insightful comments and suggestions. The authors
are grateful to the researchers who performed excel-
lent work previously and made this review possible
through papers publications and data availability.
AUThOR CONTRIbUTIONs
L.R.F.: Data curation, Visualization, Writing - original
draft, Writing - review & editing;
S.B.P.: Data curation, Writing - original draft; Statistical
analyses
L.S.M., G.M., C.G.: Data curation
R.M.L.: Conceptualization, Supervision, Writing -
review & editing;
C.N.S.: Conceptualization, Supervision, Writing -
review & editing.
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... Because temperature can affect microbial metabolic processes (López-Urrutia et al., 2006;Regaudie-de-Gioux and Duarte, 2012;Bergo et al., 2017;Frazão et al., 2021), a possible increase in DCM productivity rates was estimated due to incubation of DCM samples at surface temperature. The temperature coefficient (Q 10 ) given by Van 't Hoff's equation represents the increase in a certain reaction rate when temperature is raised by 10 K: ...
... These organisms have been reported in the Santos Basin, with higher concentrations in the warmer CW and colder TW, respectively, and with concentrations correlated with temperature (Bergo et al., 2017). Temperature has been highlighted as an important variable affecting microbial communities and processes in the South Atlantic Subtropical Gyre (Frazão et al., 2021). The lack of statistical significance between means of photosynthesis at surface and DCM (reported year-round in Santos Basin (Brandini et al., 2014)) may be associated with the presence of both layers in the same water mass in almost all stations. ...
... The deep sea, defined as the ocean lying below 200 m depth, is a highly connected environment; however, it remains undersampled, particularly in the southern hemisphere (Levin et al., 2019;Frazão et al., 2021). A recent review on microbial ecology in the ocean reported that there are only 38 studies in the ocean basins of the southern hemisphere, compared with 290 studies conducted in the North Atlantic Ocean (Frazão et al., 2021). ...
... The deep sea, defined as the ocean lying below 200 m depth, is a highly connected environment; however, it remains undersampled, particularly in the southern hemisphere (Levin et al., 2019;Frazão et al., 2021). A recent review on microbial ecology in the ocean reported that there are only 38 studies in the ocean basins of the southern hemisphere, compared with 290 studies conducted in the North Atlantic Ocean (Frazão et al., 2021). ...
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